An apoplastic peptide activates salicylic acid signalling in maize

  • Nature Plantsvolume 4pages172180 (2018)
  • doi:10.1038/s41477-018-0116-y
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Localized control of cell death is crucial for the resistance of plants to pathogens. Papain-like cysteine proteases (PLCPs) regulate plant defence to drive cell death and protection against biotrophic pathogens. In maize (Zea mays), PLCPs are crucial in the orchestration of salicylic acid (SA)-dependent defence signalling. Despite this central role in immunity, it remains unknown how PLCPs are activated, and which downstream signals they induce to trigger plant immunity. Here, we discover an immune signalling peptide, Z. mays immune signalling peptide 1 (Zip1), which is produced after salicylic acid (SA) treatment. In vitro studies demonstrate that PLCPs are required to release bioactive Zip1 from its propeptide precursor. Conversely, Zip1 treatment strongly elicits SA accumulation in leaves. Moreover, transcriptome analyses revealed that Zip1 and SA induce highly overlapping transcriptional changes. Consequently, Zip1 promotes the infection of the necrotrophic fungus Botrytis cinerea, while it reduces virulence of the biotrophic fungus Ustilago maydis. Thus, Zip1 represents the previously missing signal that is released by PLCPs to activate SA defence signalling.

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This work is funded by the German Research Foundation (DFG) via grant DO 1421/5-1 (GD). Mass spectrometry work was financially supported by an ERC starting grant (M.K., grant No. 258413) and the Deutsche Forschungsgemeinschaft (M.K., grant no. INST 20876/127-1 FUGG). Research in the Zipfel laboratory is supported by the Gatsby Charitable Foundation. We are very grateful to R. Kahmann for helpful discussions and the Max Planck Institute for Terrestrial Microbiology, Marburg, Germany, for continuous support and access to laboratory facilities. We are also very thankful to A. Matei for meaningful discussions and for critical reading the manuscript. We thank R. van der Hoorn (Oxford University) for generously providing us with ABPP probes.

Author contributions

S.Z., K.L. and G.D. designed the experiments and analysed the data. S.Z., K.L. and B.A. performed the functional analysis of Zip1/PROZIP1. N.H. and C.Z. designed and analysed ROS and MAPK assays. Y.D., A.H. and E.S. designed, performed and analysed salicylic acid measurements. U.L. analysed the transcriptome data. F.K., T.C. and M.K. performed MS experiments and MS-related data analysis. S.Z. and G.D. wrote the manuscript with input from all authors.

Author information

Author notes

    • Karina van der Linde

    Present address: Cell Biology and Plant Biochemistry, University of Regensburg, Regensburg, Germany


  1. Botanical Institute and Cluster of Excellence on Plant Sciences (CEPLAS), University of Cologne, BioCenter, Cologne, Germany

    • Sebastian Ziemann
    • , Beyda Acar
    •  & Gunther Doehlemann
  2. Department of Biology, Stanford University, Stanford, CA, USA

    • Karina van der Linde
  3. Fraunhofer Institute for Toxicology and Experimental Medicine ITEM, Division of Personalized Tumor Therapy, Regensburg, Germany

    • Urs Lahrmann
  4. Centre for Medical Biotechnology, Chemical Biology, Faculty of Biology, University Duisburg-Essen, Essen, Germany

    • Farnusch Kaschani
    •  & Markus Kaiser
  5. Max Planck Institute for Biology of Ageing, Cologne, Germany

    • Tom Colby
  6. Section of Cell and Developmental Biology, University of California at San Diego, La Jolla, CA, USA

    • Yezhang Ding
    • , Eric Schmelz
    •  & Alisa Huffaker
  7. The Sainsbury Laboratory, Norwich Research Park, Norwich, UK

    • Nicholas Holton
    •  & Cyril Zipfel


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Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Gunther Doehlemann.

Supplementary information

  1. Supplementary Information

    Supplementary Materials and Methods, Supplementary References, Supplementary Figures 1–7, Supplementary Table 2, Supplementary Table 3.

  2. Life Sciences Reporting Summary

  3. Supplementary Table 1

    Complete gene list of RNAseq analyses with differentially expressed genes in response to SA and Zip1 compared to mock samples, respectively