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Targeting Magnaporthe oryzae effector MoErs1 and host papain-like protease OsRD21 interaction to combat rice blast

Nature Plants volume 10, pages 618–632 (2024)Cite this article

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Abstract

Effector proteins secreted by plant pathogenic fungi are important artilleries against host immunity, but there is no precedent of such effectors being explored as antifungal targets. Here we demonstrate that MoErs1, a species-specific effector protein secreted by the rice blast fungus Magnaporthe oryzae, inhibits the function of rice papain-like cysteine protease OsRD21 involved in rice immunity. Disrupting MoErs1–OsRD21 interaction effectively controls rice blast. In addition, we show that FY21001, a structure–function-based designer compound, specifically binds to and inhibits MoErs1 function. FY21001 significantly and effectively controls rice blast in field tests. Our study revealed a novel concept of targeting pathogen-specific effector proteins to prevent and manage crop diseases.

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Fig. 1: MoErs1 is a cytoplastic effector required for the virulence of M. oryzae.
Fig. 2: MoErs1 interacts with OsRD21 in the plasma membrane in vivo.
Fig. 3: MoErs1 functions as a PLCP inhibitor to inhibit the activity of OsRD21.
Fig. 4: The diphenyl ether ester compound inhibits the inhibitory activity of MoErs1.
Fig. 5: Diphenyl ether ester compounds are effective against rice blast.
Fig. 6: A proposed model of MoErs1 function to suppress host immunity.

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Data availability

All data generated or analysed during this study are included in this published article and its supplementary files. Bio-reagents are available for research purposes upon request from the corresponding author under a Material Transfer Agreement. The NCBI non-redundant protein sequences (nr) database is available at https://blast.ncbi.nlm.nih.gov/Blast.cgi. The CDS sequence for the MoRES1 gene is available in the NCBI database (accession no. OK562582).

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Acknowledgements

We thank the BL17U1 staff at Shanghai Synchrotron Radiation Facility for data collection and processing, and C. Liao at Nanjing Agricultural University for model colouring. This research was supported by the National Key Research and Development Programme of China (2022YFD1700300), the key programme of the Natural Science Foundation of China (NSFC) (32030091), NSFC programme 32172377 and NSFC Youth Program 31901832. Research in P.W.’s lab was supported by the US National Institutes of Health under award numbers AI156254 and AI168867.

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  1. These authors contributed equally: Muxing Liu, Fangfang Wang, Bo He.

Authors and Affiliations

  1. Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, and Key Laboratory of Plant Immunity, Ministry of Education, Nanjing, China

    Muxing Liu, Bo He, Jiexiong Hu, Ying Dai, Weizhong Chen, Mingxi Yi, Haifeng Zhang, Yonghao Ye, Xiaobo Zheng & Zhengguang Zhang

  2. Shanghai Key Laboratory of Regulatory Biology, Institute of Biomedical Sciences and School of Life Sciences, East China Normal University, Shanghai, China

    Fangfang Wang

  3. College of Life Science, Nanjing Agricultural University, Nanjing, China

    Zhongli Cui

  4. Departments of Microbiology, Immunology and Parasitology, and Pediatrics, Louisiana State University Health Sciences Center, New Orleans, LA, USA

    Ping Wang

  5. Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, China

    Weiman Xing

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Contributions

M.L. and Z.Z. conceived and designed the study. M.L., F.W. and B.H. performed experiments with phenotypic and biochemical assays. M.L., B.H., J.H., Y.D. and W.C. contributed reagents, plant and fungal materials. M.L., F.W., B.H., M.Y., H.Z. and W.X. collected data. M.L., Y.Y., Z.C., X.Z., P.W., W.X. and Z.Z. analysed the data and wrote the paper.

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Correspondence to Weiman Xing or Zhengguang Zhang.

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Supplementary Information

Supplementary Figs. 1–22, Tables 1–3 and 5–8, and key resources table.

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Supplementary Table 4

Sequence of MoERS1 gene in various rice blast isolates.

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Liu, M., Wang, F., He, B. et al. Targeting Magnaporthe oryzae effector MoErs1 and host papain-like protease OsRD21 interaction to combat rice blast. Nat. Plants 10, 618–632 (2024). https://doi.org/10.1038/s41477-024-01642-x

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