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Attenuation of phytofungal pathogenicity of Ascomycota by autophagy modulators

Author

Listed:
  • Jongchan Woo

    (University of California
    University of Wyoming
    Seoul National University)

  • Seungmee Jung

    (University of Wyoming)

  • Seongbeom Kim

    (Seoul National University)

  • Yurong Li

    (Texas A & M University
    Corteva Agriscience)

  • Hyunjung Chung

    (Seoul National University)

  • Tatiana V. Roubtsova

    (University of California)

  • Honghong Zhang

    (Texas A & M University
    Fujian Agriculture and Forestry University)

  • Celine Caseys

    (University of California)

  • Dan Kliebenstein

    (University of California)

  • Kyung-Nam Kim

    (Sejong University)

  • Richard M. Bostock

    (University of California)

  • Yong-Hwan Lee

    (Seoul National University)

  • Martin B. Dickman

    (Texas A & M University)

  • Doil Choi

    (Seoul National University)

  • Eunsook Park

    (University of Wyoming)

  • Savithramma P. Dinesh-Kumar

    (University of California)

Abstract

Autophagy in eukaryotes functions to maintain homeostasis by degradation and recycling of long-lived and unwanted cellular materials. Autophagy plays important roles in pathogenicity of various fungal pathogens, suggesting that autophagy is a novel target for development of antifungal compounds. Here, we describe bioluminescence resonance energy transfer (BRET)-based high-throughput screening (HTS) strategy to identify compounds that inhibit fungal ATG4 cysteine protease-mediated cleavage of ATG8 that is critical for autophagosome formation. We identified ebselen (EB) and its analogs ebselen oxide (EO) and 2-(4-methylphenyl)−1,2-benzisothiazol-3(2H)-one (PT) as inhibitors of fungal pathogens Botrytis cinerea and Magnaporthe oryzae ATG4-mediated ATG8 processing. The EB and its analogs inhibit spore germination, hyphal development, and appressorium formation in Ascomycota pathogens, B. cinerea, M. oryzae, Sclerotinia sclerotiorum and Monilinia fructicola. Treatment with EB and its analogs significantly reduced fungal pathogenicity. Our findings provide molecular insights to develop the next generation of antifungal compounds by targeting autophagy in important fungal pathogens.

Suggested Citation

  • Jongchan Woo & Seungmee Jung & Seongbeom Kim & Yurong Li & Hyunjung Chung & Tatiana V. Roubtsova & Honghong Zhang & Celine Caseys & Dan Kliebenstein & Kyung-Nam Kim & Richard M. Bostock & Yong-Hwan Le, 2024. "Attenuation of phytofungal pathogenicity of Ascomycota by autophagy modulators," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45839-2
    DOI: 10.1038/s41467-024-45839-2
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    1. Yoshinobu Ichimura & Takayoshi Kirisako & Toshifumi Takao & Yoshinori Satomi & Yasutsugu Shimonishi & Naotada Ishihara & Noboru Mizushima & Isei Tanida & Eiki Kominami & Mariko Ohsumi & Takeshi Noda &, 2000. "A ubiquitin-like system mediates protein lipidation," Nature, Nature, vol. 408(6811), pages 488-492, November.
    2. Ralph A. Dean & Nicholas J. Talbot & Daniel J. Ebbole & Mark L. Farman & Thomas K. Mitchell & Marc J. Orbach & Michael Thon & Resham Kulkarni & Jin-Rong Xu & Huaqin Pan & Nick D. Read & Yong-Hwan Lee , 2005. "The genome sequence of the rice blast fungus Magnaporthe grisea," Nature, Nature, vol. 434(7036), pages 980-986, April.
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