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Chloroplasts play a central role in plant defence and are targeted by pathogen effectors

Nature Plants volume 1, Article number: 15074 (2015) Cite this article

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Abstract

Microbe associated molecular pattern (MAMP) receptors in plants recognize MAMPs and activate basal defences; however a complete understanding of the molecular and physiological mechanisms conferring immunity remains elusive. Pathogens suppress active defence in plants through the combined action of effector proteins. Here we show that the chloroplast is a key component of early immune responses. MAMP perception triggers the rapid, large-scale suppression of nuclear encoded chloroplast-targeted genes (NECGs). Virulent Pseudomonas syringae effectors reprogramme NECG expression in Arabidopsis, target the chloroplast and inhibit photosynthetic CO2 assimilation through disruption of photosystem II. This activity prevents a chloroplastic reactive oxygen burst. These physiological changes precede bacterial multiplication and coincide with pathogen-induced abscisic acid (ABA) accumulation. MAMP pretreatment protects chloroplasts from effector manipulation, whereas application of ABA or the inhibitor of photosynthetic electron transport, DCMU, abolishes the MAMP-induced chloroplastic reactive oxygen burst, and enhances growth of a P. syringae hrpA mutant that fails to secrete effectors.

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Figure 1: Nuclear encoded chloroplast transcript dynamics in defence and disease responses to Pseudomonas syringae pv. tomato DC3000.
Figure 2: Pseudomonas syringae DC3000 rapidly inhibits photosynthesis in Arabidopsis thaliana.
Figure 3: DC3000 effectors suppress Fv/Fm, in an ABA dependent manner.
Figure 4: Chloroplast localized HopN1 and HopI1 do not modify Fv/Fm.
Figure 5: Effector suppression of a photosynthesis-derived reactive species burst is necessary to overcome basal defences and promote pathogen growth.

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Acknowledgements

This work was funded by BBSRC grants BB/E010334/1 to M.G. and BB/F005903/1 to M.G. and N.S. M.T. and D.L. thank R. Bock and the Max Planck Society (MPG) for their support. We are indebted to members of the PRESTA consortium for their efforts in generating the microarray data. We thank J. Greenberg for the Pma4326 hopI1 strain and E. Lopez-Solanilla for the HopN1 derivatives. We are indebted to K. Polanski for generating the images for Fig. 1b and Alan Collmer for Pf55, CUCPB6032 and ΔfliC strains.

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Authors and Affiliations

  1. Biosciences, College of Life and Environment Sciences, University of Exeter, Exeter, EX4 4QD, UK

    Marta de Torres Zabala, George Littlejohn, Siddharth Jayaraman, David Studholme, Trevor Bailey, Nicholas Smirnoff & Murray Grant

  2. School of Biological Sciences, University of Essex, Colchester, CO4 3SQ, UK

    Tracy Lawson

  3. Max Planck Institute of Molecular Plant Physiology, Am Müehlenberg 1, Potsdam-Golm, D-14476, Germany

    Michael Tillich & Dirk Licht

  4. Department of Biology I, Botany, Ludwig-Maximilians-Universität München, Groβhaderner Strase 2–4, Planegg-Martinsried, D-82152, Germany

    Bettina Bölter & Laura Delfino

  5. Department of Plant Biology, University of Minnesota, USA

    William Truman

  6. Department of Life Sciences, Imperial College, London, SW7 2AZ, UK

    John Mansfield

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Contributions

M.G., M.d.T., J.M., M.T. and N.S. conceived the experiments, M.T., D.L., L.D. and B.B. undertook the chloroplast localization and effector predictions, S.J., T.B. and D.S. the bioinformatics, T.L., N.S. the photosynthesis experiments, G.L. the microscopy and M.d.T. and W.T. contributed to the remainder of the experimental work. M.d.T., M.G., N.S., J.M. and M.T. wrote the manuscript.

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Correspondence to Murray Grant.

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de Torres Zabala, M., Littlejohn, G., Jayaraman, S. et al. Chloroplasts play a central role in plant defence and are targeted by pathogen effectors. Nature Plants 1, 15074 (2015). https://doi.org/10.1038/nplants.2015.74

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