IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-46903-7.html
   My bibliography  Save this article

A fungal core effector exploits the OsPUX8B.2–OsCDC48-6 module to suppress plant immunity

Author

Listed:
  • Xuetao Shi

    (Chinese Academy of Agricultural Sciences
    Chinese Academy of Agricultural Sciences)

  • Xin Xie

    (Chinese Academy of Agricultural Sciences)

  • Yuanwen Guo

    (Chinese Academy of Agricultural Sciences)

  • Junqi Zhang

    (Chinese Academy of Agricultural Sciences)

  • Ziwen Gong

    (Chinese Academy of Agricultural Sciences
    Chinese Academy of Agricultural Sciences)

  • Kai Zhang

    (Chinese Academy of Agricultural Sciences)

  • Jie Mei

    (Chinese Academy of Agricultural Sciences
    Chinese Academy of Agricultural Sciences)

  • Xinyao Xia

    (Chinese Academy of Agricultural Sciences)

  • Haoxue Xia

    (Chinese Academy of Agricultural Sciences)

  • Na Ning

    (Chinese Academy of Agricultural Sciences)

  • Yutao Xiao

    (Chinese Academy of Agricultural Sciences)

  • Qing Yang

    (Chinese Academy of Agricultural Sciences)

  • Guo-Liang Wang

    (The Ohio State University)

  • Wende Liu

    (Chinese Academy of Agricultural Sciences)

Abstract

Proteins containing a ubiquitin regulatory X (UBX) domain are cofactors of Cell Division Cycle 48 (CDC48) and function in protein quality control. However, whether and how UBX-containing proteins participate in host–microbe interactions remain unclear. Here we show that MoNLE1, an effector from the fungal pathogen Magnaporthe oryzae, is a core virulence factor that suppresses rice immunity by specifically interfering with OsPUX8B.2. The UBX domain of OsPUX8B.2 is required for its binding to OsATG8 and OsCDC48-6 and controls its 26 S proteasome–dependent stability. OsPUX8B.2 and OsCDC48-6 positively regulate plant immunity against blast fungus, while the high-temperature tolerance heat-shock protein OsBHT, a putative cytoplasmic substrate of OsPUX8B.2–OsCDC48-6, negatively regulates defense against blast infection. MoNLE1 promotes the nuclear migration and degradation of OsPUX8B.2 and disturbs its association with OsBHT. Given the high conservation of MoNLE1 among fungal isolates, plants with broad and durable blast resistance might be generated by engineering intracellular proteins resistant to MoNLE1.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46903-7
    DOI: 10.1038/s41467-024-46903-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-46903-7
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-46903-7?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. Yuri Shibata & Masaaki Oyama & Hiroko Kozuka-Hata & Xiao Han & Yuetsu Tanaka & Jin Gohda & Jun-ichiro Inoue, 2012. "p47 negatively regulates IKK activation by inducing the lysosomal degradation of polyubiquitinated NEMO," Nature Communications, Nature, vol. 3(1), pages 1-13, January.
    2. Seongbeom Kim & Chi-Yeol Kim & Sook-Young Park & Ki-Tae Kim & Jongbum Jeon & Hyunjung Chung & Gobong Choi & Seomun Kwon & Jaeyoung Choi & Junhyun Jeon & Jong-Seong Jeon & Chang Hyun Khang & Seogchan K, 2020. "Two nuclear effectors of the rice blast fungus modulate host immunity via transcriptional reprogramming," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    3. 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.
    4. Yongliang Zhang & Gaoyuan Song & Neeraj K. Lal & Ugrappa Nagalakshmi & Yuanyuan Li & Wenjie Zheng & Pin-jui Huang & Tess C. Branon & Alice Y. Ting & Justin W. Walley & Savithramma P. Dinesh-Kumar, 2019. "TurboID-based proximity labeling reveals that UBR7 is a regulator of N NLR immune receptor-mediated immunity," Nature Communications, Nature, vol. 10(1), pages 1-17, December.
    5. Aobo Huang & Yu Tang & Xuetao Shi & Min Jia & Jinheng Zhu & Xiaohan Yan & Huiqin Chen & Yangnan Gu, 2020. "Proximity labeling proteomics reveals critical regulators for inner nuclear membrane protein degradation in plants," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    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. 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.
    3. 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.
    4. Xue-Ming Wu & Bo-Sen Zhang & Yun-Long Zhao & Hua-Wei Wu & Feng Gao & Jie Zhang & Jian-Hua Zhao & Hui-Shan Guo, 2023. "DeSUMOylation of a Verticillium dahliae enolase facilitates virulence by derepressing the expression of the effector VdSCP8," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    5. 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.
    6. Zongyu Gao & Dingliang Zhang & Xiaoling Wang & Xin Zhang & Zhiyan Wen & Qianshen Zhang & Dawei Li & Savithramma P. Dinesh-Kumar & Yongliang Zhang, 2022. "Coat proteins of necroviruses target 14-3-3a to subvert MAPKKKα-mediated antiviral immunity in plants," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    7. Ziwei Zhu & Jun Xiong & Hao Shi & Yuchen Liu & Junjie Yin & Kaiwei He & Tianyu Zhou & Liting Xu & Xiaobo Zhu & Xiang Lu & Yongyan Tang & Li Song & Qingqing Hou & Qing Xiong & Long Wang & Daihua Ye & T, 2023. "Magnaporthe oryzae effector MoSPAB1 directly activates rice Bsr-d1 expression to facilitate pathogenesis," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    8. Yang Xu & Han Han & Ian Cooney & Yuxuan Guo & Noah G. Moran & Nathan R. Zuniga & John C. Price & Christopher P. Hill & Peter S. Shen, 2022. "Active conformation of the p97-p47 unfoldase complex," Nature Communications, Nature, vol. 13(1), pages 1-8, December.
    9. 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.
    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. 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_s41467-024-46903-7. 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.