IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-45839-2.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-45839-2
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-45839-2?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Jun Huang & David Rowe & Pratima Subedi & Wei Zhang & Tyler Suelter & Barbara Valent & David E. Cook, 2022. "CRISPR-Cas12a induced DNA double-strand breaks are repaired by multiple pathways with different mutation profiles in Magnaporthe oryzae," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    2. Yogesh K. Gupta & Francismar C. Marcelino-Guimarães & Cécile Lorrain & Andrew Farmer & Sajeet Haridas & Everton Geraldo Capote Ferreira & Valéria S. Lopes-Caitar & Liliane Santana Oliveira & Emmanuell, 2023. "Major proliferation of transposable elements shaped the genome of the soybean rust pathogen Phakopsora pachyrhizi," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    3. Xuetao Shi & Xin Xie & Yuanwen Guo & Junqi Zhang & Ziwen Gong & Kai Zhang & Jie Mei & Xinyao Xia & Haoxue Xia & Na Ning & Yutao Xiao & Qing Yang & Guo-Liang Wang & Wende Liu, 2024. "A fungal core effector exploits the OsPUX8B.2–OsCDC48-6 module to suppress plant immunity," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    4. Kuninori Suzuki & Shingo Nakamura & Mayumi Morimoto & Kiyonaga Fujii & Nobuo N Noda & Fuyuhiko Inagaki & Yoshinori Ohsumi, 2014. "Proteomic Profiling of Autophagosome Cargo in Saccharomyces cerevisiae," PLOS ONE, Public Library of Science, vol. 9(3), pages 1-9, March.
    5. M. O. Aremu & Hashim Ibrahim, 2017. "Dietary Phospholipids and Phytostrerols: A Review on Some Nigerian Vegetable Oils," International Journal of Sciences, Office ijSciences, vol. 6(09), pages 94-102, September.
    6. Kai-Chih Hung & Hui-Ju Huang & Ming-Wei Lin & Yen-Ping Lei & Anya Maan-yuh Lin, 2014. "Roles of Autophagy in MPP+-Induced Neurotoxicity In Vivo: The Involvement of Mitochondria and α-Synuclein Aggregation," PLOS ONE, Public Library of Science, vol. 9(3), pages 1-9, March.
    7. Yuki Takakura & Moeka Machida & Natsumi Terada & Yuka Katsumi & Seika Kawamura & Kenta Horie & Maki Miyauchi & Tatsuya Ishikawa & Nobuko Akiyama & Takao Seki & Takahisa Miyao & Mio Hayama & Rin Endo &, 2024. "Mitochondrial protein C15ORF48 is a stress-independent inducer of autophagy that regulates oxidative stress and autoimmunity," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    8. Hang Liu & Xunli Lu & Mengfei Li & Zhiqin Lun & Xia Yan & Changfa Yin & Guixin Yuan & Xingbin Wang & Ning Liu & Di Liu & Mian Wu & Ziluolong Luo & Yan Zhang & Vijai Bhadauria & Jun Yang & Nicholas J. , 2023. "Plant immunity suppression by an exo-β-1,3-glucanase and an elongation factor 1α of the rice blast fungus," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    9. Barbara Baldo & Rana Soylu & Åsa Petersén, 2013. "Maintenance of Basal Levels of Autophagy in Huntington’s Disease Mouse Models Displaying Metabolic Dysfunction," PLOS ONE, Public Library of Science, vol. 8(12), pages 1-15, December.
    10. Gang Li & Ziwen Gong & Nawaraj Dulal & Margarita Marroquin-Guzman & Raquel O. Rocha & Michael Richter & Richard A. Wilson, 2023. "A protein kinase coordinates cycles of autophagy and glutaminolysis in invasive hyphae of the fungus Magnaporthe oryzae within rice cells," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    11. Hayden Weng Siong Tan & Guang Lu & Han Dong & Yik-Lam Cho & Auginia Natalia & Liming Wang & Charlene Chan & Dennis Kappei & Reshma Taneja & Shuo-Chien Ling & Huilin Shao & Shih-Yin Tsai & Wen-Xing Din, 2022. "A degradative to secretory autophagy switch mediates mitochondria clearance in the absence of the mATG8-conjugation machinery," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    12. Md Azadul Haque & Mohd Y. Rafii & Martini Mohammad Yusoff & Nusaibah Syd Ali & Oladosu Yusuff & Debi Rani Datta & Mohammad Anisuzzaman & Mohammad Ferdous Ikbal, 2021. "Recent Advances in Rice Varietal Development for Durable Resistance to Biotic and Abiotic Stresses through Marker-Assisted Gene Pyramiding," Sustainability, MDPI, vol. 13(19), pages 1-25, September.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45839-2. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.