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Timing of plant immune responses by a central circadian regulator

Abstract

The principal immune mechanism against biotrophic pathogens in plants is the resistance (R)-gene-mediated defence1. It was proposed to share components with the broad-spectrum basal defence machinery2. However, the underlying molecular mechanism is largely unknown. Here we report the identification of novel genes involved in R-gene-mediated resistance against downy mildew in Arabidopsis and their regulatory control by the circadian regulator, CIRCADIAN CLOCK-ASSOCIATED 1 (CCA1). Numerical clustering based on phenotypes of these gene mutants revealed that programmed cell death (PCD) is the major contributor to resistance. Mutants compromised in the R-gene-mediated PCD were also defective in basal resistance, establishing an interconnection between these two distinct defence mechanisms. Surprisingly, we found that these new defence genes are under circadian control by CCA1, allowing plants to ‘anticipate’ infection at dawn when the pathogen normally disperses the spores and time immune responses according to the perception of different pathogenic signals upon infection. Temporal control of the defence genes by CCA1 differentiates their involvement in basal and R-gene-mediated defence. Our study has revealed a key functional link between the circadian clock and plant immunity.

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Figure 1: Phenotypic analyses discovered two distinct RPP4-mediated resistance responses against Hpa Emwa1.
Figure 2: Some of the RPP4-mediated resistance mutants are also compromised in basal defence.
Figure 3: The circadian regulator, CCA1, controls the defence gene expression and the timing of immune responses.

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Primary accessions

Gene Expression Omnibus

Data deposits

The microarray data presented in this publication have been deposited in NCBI's Gene Expression Omnibus and are accessible through GEO Series accession number GSE22274.

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Acknowledgements

We thank S. Brady for performing mixed model ANOVA of the data and advice on data analyses; J. Li for sharing the protocol for elf18 treatment, E. Tobin for providing the CCA1OE transgenic line, R. McClung for CCA1:LUC, LHY:LUC, ztl-4 lines. H. Lu for helpful discussion of the work, F. Ausubel, P. Benfey, S. Brady, J. Siedow and R. Mohan for critiquing the manuscript. This work was supported by a grant from NSF (MCB-0519898) to X.D. and a grant (HG004659) to X.-D.F.

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J.Y.B., W.W., Y.T., D.C. and D.-u.L. identified new components in R-gene-mediated resistance; J.Y.B., W.W. and Y.T. showed that RPP4 controls two major defence responses by phenotypic clustering analysis; J.Y.B., W.W. and M.T. demonstrated that R-gene-mediated resistance shares common components with basal defence machinery; W.W., J.Y.B., H.L., X.-D.F. and X.D. verified the circadian regulator CCA1 plays a key role in timing the different immune responses; W.W., J.Y.B. and X.D. wrote the manuscript with inputs from all co-authors. All authors discussed the results and commented on the manuscript.

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Correspondence to Xinnian Dong.

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The authors declare no competing financial interests.

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This file contains Supplementary Figures 1-12 with legends and Supplementary Tables 1-3. (PDF 2349 kb)

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Wang, W., Barnaby, J., Tada, Y. et al. Timing of plant immune responses by a central circadian regulator. Nature 470, 110–114 (2011). https://doi.org/10.1038/nature09766

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