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Timing of plant immune responses by a central circadian regulator

Nature volume 470, pages 110–114 (2011)Cite this article

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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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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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Author notes

  1. Jinyoung Yang Barnaby

    Present address: Present address: Crop Systems and Global Change Laboratory, United States Department of Agriculture, Agricultural Research Service, Plant Sciences Institute, Room 342, Building 001, BARC-West, 10300 Baltimore Avenue, Beltsville, Maryland 20705,USA,

  2. Yasuomi Tada

    Present address: Present address: Life Science Research Centre, Institute of Research Promotion, Kagawa University, 2393 Ikenobe, Miki-cho, Kita-gun, Kagawa 761-0795, Japan,

  3. Daniela Caldelari

    Present address: Present address: Plant Molecular Biology, University of Lausanne, CH-1015 Lausanne, Switzerland,

  4. Wei Wang and Jinyoung Yang Barnaby: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Biology, P. O. Box 90338, Duke University, Durham, 27708, North Carolina, USA

    Wei Wang, Jinyoung Yang Barnaby, Yasuomi Tada, Daniela Caldelari, Dae-un Lee & Xinnian Dong

  2. Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, California 92093, USA,

    Hairi Li & Xiang-Dong Fu

  3. National Pollen and Aerobiology Research Unit (NPARU), University of Worcester, Henwick Grove, Worcester WR2 6AJ, UK ,

    Mahmut Tör

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Contributions

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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