IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-46290-z.html
   My bibliography  Save this article

PsAF5 functions as an essential adapter for PsPHB2-mediated mitophagy under ROS stress in Phytophthora sojae

Author

Listed:
  • Wenhao Li

    (Northwest A&F University)

  • Hongwei Zhu

    (Northwest A&F University)

  • Jinzhu Chen

    (Northwest A&F University)

  • Binglu Ru

    (Northwest A&F University)

  • Qin Peng

    (Northwest A&F University)

  • Jianqiang Miao

    (Northwest A&F University)

  • Xili Liu

    (Northwest A&F University
    China Agricultural University)

Abstract

Host-derived reactive oxygen species (ROS) are an important defense means to protect against pathogens. Although mitochondria are the main intracellular targets of ROS, how pathogens regulate mitochondrial physiology in response to oxidative stress remains elusive. Prohibitin 2 (PHB2) is an inner mitochondrial membrane (IMM) protein, recognized as a mitophagy receptor in animals and fungi. Here, we find that an ANK and FYVE domain-containing protein PsAF5, is an adapter of PsPHB2, interacting with PsATG8 under ROS stress. Unlike animal PHB2 that can recruit ATG8 directly to mitochondria, PsPHB2 in Phytophthora sojae cannot recruit PsATG8 to stressed mitochondria without PsAF5. PsAF5 deletion impairs mitophagy under ROS stress and increases the pathogen’s sensitivity to H2O2, resulting in the attenuation of P. sojae virulence. This discovery of a PsPHB2-PsATG8 adapter (PsAF5) in plant-pathogenic oomycetes reveals that mitophagy induction by IMM proteins is conserved in eukaryotes, but with differences in the details of ATG8 recruitment.

Suggested Citation

  • Wenhao Li & Hongwei Zhu & Jinzhu Chen & Binglu Ru & Qin Peng & Jianqiang Miao & Xili Liu, 2024. "PsAF5 functions as an essential adapter for PsPHB2-mediated mitophagy under ROS stress in Phytophthora sojae," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46290-z
    DOI: 10.1038/s41467-024-46290-z
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-46290-z
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-46290-z?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. Bruno Pok Man Ngou & Hee-Kyung Ahn & Pingtao Ding & Jonathan D. G. Jones, 2021. "Mutual potentiation of plant immunity by cell-surface and intracellular receptors," Nature, Nature, vol. 592(7852), pages 110-115, April.
    2. Jonathan D. G. Jones & Jeffery L. Dangl, 2006. "The plant immune system," Nature, Nature, vol. 444(7117), pages 323-329, November.
    3. Xiaoli Zhang & Xiping Cheng & Lu Yu & Junsheng Yang & Raul Calvo & Samarjit Patnaik & Xin Hu & Qiong Gao & Meimei Yang & Maria Lawas & Markus Delling & Juan Marugan & Marc Ferrer & Haoxing Xu, 2016. "MCOLN1 is a ROS sensor in lysosomes that regulates autophagy," Nature Communications, Nature, vol. 7(1), pages 1-12, November.
    4. Yuko Fujioka & Jahangir Md. Alam & Daisuke Noshiro & Kazunari Mouri & Toshio Ando & Yasushi Okada & Alexander I. May & Roland L. Knorr & Kuninori Suzuki & Yoshinori Ohsumi & Nobuo N. Noda, 2020. "Phase separation organizes the site of autophagosome formation," Nature, Nature, vol. 578(7794), pages 301-305, February.
    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. Sheng Yang & Weiwei Cai & Ruijie Wu & Yu Huang & Qiaoling Lu & Hui Wang & Xueying Huang & Yapeng Zhang & Qing Wu & Xingge Cheng & Meiyun Wan & Jingang Lv & Qian Liu & Xiang Zheng & Shaoliang Mou & Dey, 2023. "Differential CaKAN3-CaHSF8 associations underlie distinct immune and heat responses under high temperature and high humidity conditions," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Jiahui Liu & Xiaoyun Wu & Yue Fang & Ye Liu & Esther Oreofe Bello & Yong Li & Ruyi Xiong & Yinzi Li & Zheng Qing Fu & Aiming Wang & Xiaofei Cheng, 2023. "A plant RNA virus inhibits NPR1 sumoylation and subverts NPR1-mediated plant immunity," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    3. Paul Vincelli, 2016. "Genetic Engineering and Sustainable Crop Disease Management: Opportunities for Case-by-Case Decision-Making," Sustainability, MDPI, vol. 8(5), pages 1-22, May.
    4. Norliza Abu-Bakar & Nor Mustaiqazah Juri & Ros Azrinawati Hana Abu-Bakar & Mohd Zulfadli Sohaime & Rafidah Badrun & Johari Sarip & Mohd Azhar Hassan & Khairulmazmi Ahmad, 2021. "Recombinant Protein Foliar Application Activates Systemic Acquired Resistance and Increases Tolerance against Papaya Dieback Disease," Asian Journal of Agriculture and rural Development, Asian Economic and Social Society, vol. 11(1), pages 1-9, March.
    5. Xin Tong & Jia-Jia Zhao & Ya-Lan Feng & Jing-Ze Zou & Jian Ye & Junfeng Liu & Chenggui Han & Dawei Li & Xian-Bing Wang, 2023. "A selective autophagy receptor VISP1 induces symptom recovery by targeting viral silencing suppressors," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    6. Huanhuan Li & Wenqiang Men & Chao Ma & Qianwen Liu & Zhenjie Dong & Xiubin Tian & Chaoli Wang & Cheng Liu & Harsimardeep S. Gill & Pengtao Ma & Zhibin Zhang & Bao Liu & Yue Zhao & Sunish K. Sehgal & W, 2024. "Wheat powdery mildew resistance gene Pm13 encodes a mixed lineage kinase domain-like protein," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    7. Farhan Ali & Qingchun Pan & Genshen Chen & Kashif Rafiq Zahid & Jianbing Yan, 2013. "Evidence of Multiple Disease Resistance (MDR) and Implication of Meta-Analysis in Marker Assisted Selection," PLOS ONE, Public Library of Science, vol. 8(7), pages 1-12, July.
    8. Jincai Qiu & Yongshan Chen & Ying Feng & Xiaofeng Li & Jinghua Xu & Jinping Jiang, 2023. "Adaptation of Rhizosphere Microbial Communities to Continuous Exposure to Multiple Residual Antibiotics in Vegetable Farms," IJERPH, MDPI, vol. 20(4), pages 1-15, February.
    9. Arsheed H. Sheikh & Iosif Zacharia & Alonso J. Pardal & Ana Dominguez-Ferreras & Daniela J. Sueldo & Jung-Gun Kim & Alexi Balmuth & Jose R. Gutierrez & Brendon F. Conlan & Najeeb Ullah & Olivia M. Nip, 2023. "Dynamic changes of the Prf/Pto tomato resistance complex following effector recognition," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    10. Karine de Guillen & Diana Ortiz-Vallejo & Jérome Gracy & Elisabeth Fournier & Thomas Kroj & André Padilla, 2015. "Structure Analysis Uncovers a Highly Diverse but Structurally Conserved Effector Family in Phytopathogenic Fungi," PLOS Pathogens, Public Library of Science, vol. 11(10), pages 1-27, October.
    11. Shuang-zhou Peng & Xiao-hui Chen & Si-jie Chen & Jie Zhang & Chuan-ying Wang & Wei-rong Liu & Duo Zhang & Ying Su & Xiao-kun Zhang, 2021. "Phase separation of Nur77 mediates celastrol-induced mitophagy by promoting the liquidity of p62/SQSTM1 condensates," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    12. Veronika DUMALASOVÁ & Leona SVOBODOVÁ & Alena HANZALOVÁ, 2012. "Differentially expressed gene transcripts in wheat and barley leaves upon leaf spot infection," Czech Journal of Genetics and Plant Breeding, Czech Academy of Agricultural Sciences, vol. 48(3), pages 108-119.
    13. Mariam Amouzoune & Sajid Rehman & Rachid Benkirane & Swati Verma & Sanjaya Gyawali & Muamar Al-Jaboobi & Ramesh Pal Singh Verma & Zakaria Kehel & Ahmed Amri, 2022. "Genome-Wide Association Study of Leaf Rust Resistance at Seedling and Adult Plant Stages in a Global Barley Panel," Agriculture, MDPI, vol. 12(11), pages 1-26, November.
    14. Baokuan Xu & Xiyan Liu & Xuejiao Song & Qifang Guo & Yongqi Yin & Chunqing Zhang & Yan Li, 2022. "High-Vigor Maize Seeds Resist Fusarium graminearum Infection through Stronger Ca 2+ Signaling," Agriculture, MDPI, vol. 12(7), pages 1-15, July.
    15. Shota Iwasaki & Naoko Okada & Yutaka Kimura & Yoshihiro Takikawa & Tomoko Suzuki & Koji Kakutani & Yoshinori Matsuda & Yuling Bai & Teruo Nonomura, 2022. "Simultaneous Detection of Plant- and Fungus-Derived Genes Constitutively Expressed in Single Pseudoidium neolycopersici -Inoculated Type I Trichome Cells of Tomato Leaves via Multiplex RT-PCR and Nest," Agriculture, MDPI, vol. 12(2), pages 1-16, February.
    16. Lauren Brzozowski & Michael Mazourek, 2018. "A Sustainable Agricultural Future Relies on the Transition to Organic Agroecological Pest Management," Sustainability, MDPI, vol. 10(6), pages 1-25, June.
    17. Chantal Gascuel & Michèle Tixier-Boichard & Benoit Dedieu & Cécile Détang-Dessendre & Pierre Dupraz & Philippe Faverdin & Laurent Hazard & Philippe Hinsinger & Isabelle Litrico-Chiarelli & Françoise M, 2019. "Réflexion prospective interdisciplinaire pour l’agroécologie. Rapport de synthèse," Post-Print hal-02154433, HAL.
    18. Deepak D. Bhandari & Dae Kwan Ko & Sang-Jin Kim & Kinya Nomura & Sheng Yang He & Federica Brandizzi, 2023. "Defense against phytopathogens relies on efficient antimicrobial protein secretion mediated by the microtubule-binding protein TGNap1," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    19. Salvatore Cosentino & Mette Voldby Larsen & Frank Møller Aarestrup & Ole Lund, 2013. "PathogenFinder - Distinguishing Friend from Foe Using Bacterial Whole Genome Sequence Data," PLOS ONE, Public Library of Science, vol. 8(10), pages 1-11, October.
    20. Wei Wei & Liangsheng Xu & Hao Peng & Wenjun Zhu & Kiwamu Tanaka & Jiasen Cheng & Karen A. Sanguinet & George Vandemark & Weidong Chen, 2022. "A fungal extracellular effector inactivates plant polygalacturonase-inhibiting protein," Nature Communications, Nature, vol. 13(1), pages 1-15, December.

    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_s41467-024-46290-z. 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.