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A fungal substrate mimicking molecule suppresses plant immunity via an inter-kingdom conserved motif

Author

Listed:
  • Johana C. Misas Villamil

    (University of Cologne)

  • André N. Mueller

    (Max Planck Institute for Terrestrial Microbiology)

  • Fatih Demir

    (Forschungszentrum Jülich)

  • Ute Meyer

    (University of Cologne)

  • Bilal Ökmen

    (University of Cologne)

  • Jan Schulze Hüynck

    (University of Cologne)

  • Marlen Breuer

    (Max Planck Institute for Terrestrial Microbiology)

  • Helen Dauben

    (University of Cologne)

  • Joe Win

    (The Sainsbury Laboratory, Norwich Research Park)

  • Pitter F. Huesgen

    (Forschungszentrum Jülich
    University of Cologne)

  • Gunther Doehlemann

    (University of Cologne)

Abstract

Ustilago maydis is a biotrophic fungus causing corn smut disease in maize. The secreted effector protein Pit2 is an inhibitor of papain-like cysteine proteases (PLCPs) essential for virulence. Pit2 inhibitory function relies on a conserved 14 amino acids motif (PID14). Here we show that synthetic PID14 peptides act more efficiently as PLCP inhibitors than the full-length Pit2 effector. Mass spectrometry shows processing of Pit2 by maize PLCPs, which releases an inhibitory core motif from the PID14 sequence. Mutational analysis demonstrates that two conserved residues are essential for Pit2 function. We propose that the Pit2 effector functions as a substrate mimicking molecule: Pit2 is a suitable substrate for apoplastic PLCPs and its processing releases the embedded inhibitor peptide, which in turn blocks PLCPs to modulate host immunity. Remarkably, the PID14 core motif is present in several plant associated fungi and bacteria, indicating the existence of a conserved microbial inhibitor of proteases (cMIP).

Suggested Citation

  • Johana C. Misas Villamil & André N. Mueller & Fatih Demir & Ute Meyer & Bilal Ökmen & Jan Schulze Hüynck & Marlen Breuer & Helen Dauben & Joe Win & Pitter F. Huesgen & Gunther Doehlemann, 2019. "A fungal substrate mimicking molecule suppresses plant immunity via an inter-kingdom conserved motif," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-09472-8
    DOI: 10.1038/s41467-019-09472-8
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    Cited by:

    1. Yu-Han Lin & Meng-Yun Xu & Chuan-Chih Hsu & Florensia Ariani Damei & Hui-Chun Lee & Wei-Lun Tsai & Cuong V. Hoang & Yin-Ru Chiang & Lay-Sun Ma, 2023. "Ustilago maydis PR-1-like protein has evolved two distinct domains for dual virulence activities," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    2. Weiliang Zuo & Jasper R. L. Depotter & Sara Christina Stolze & Hirofumi Nakagami & Gunther Doehlemann, 2023. "A transcriptional activator effector of Ustilago maydis regulates hyperplasia in maize during pathogen-induced tumor formation," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

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