IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-39426-0.html
   My bibliography  Save this article

A selective autophagy receptor VISP1 induces symptom recovery by targeting viral silencing suppressors

Author

Listed:
  • Xin Tong

    (China Agricultural University
    China Agricultural University)

  • Jia-Jia Zhao

    (China Agricultural University)

  • Ya-Lan Feng

    (China Agricultural University)

  • Jing-Ze Zou

    (China Agricultural University)

  • Jian Ye

    (Institute of Microbiology, Chinese Academy of Sciences)

  • Junfeng Liu

    (China Agricultural University)

  • Chenggui Han

    (China Agricultural University)

  • Dawei Li

    (China Agricultural University)

  • Xian-Bing Wang

    (China Agricultural University)

Abstract

Selective autophagy is a double-edged sword in antiviral immunity and regulated by various autophagy receptors. However, it remains unclear how to balance the opposite roles by one autophagy receptor. We previously identified a virus-induced small peptide called VISP1 as a selective autophagy receptor that facilitates virus infections by targeting components of antiviral RNA silencing. However, we show here that VISP1 can also inhibit virus infections by mediating autophagic degradation of viral suppressors of RNA silencing (VSRs). VISP1 targets the cucumber mosaic virus (CMV) 2b protein for degradation and attenuates its suppression activity on RNA silencing. Knockout and overexpression of VISP1 exhibit compromised and enhanced resistance against late infection of CMV, respectively. Consequently, VISP1 induces symptom recovery from CMV infection by triggering 2b turnover. VISP1 also targets the C2/AC2 VSRs of two geminiviruses and enhances antiviral immunity. Together, VISP1 induces symptom recovery from severe infections of plant viruses through controlling VSR accumulation.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39426-0
    DOI: 10.1038/s41467-023-39426-0
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-39426-0
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-39426-0?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. Si Liu & Meijuan Chen & Ruidong Li & Wan-Xiang Li & Amit Gal-On & Zhenyu Jia & Shou-Wei Ding, 2022. "Identification of positive and negative regulators of antiviral RNA interference in Arabidopsis thaliana," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    2. Jonathan D. G. Jones & Jeffery L. Dangl, 2006. "The plant immune system," Nature, Nature, vol. 444(7117), pages 323-329, November.
    3. Fangfang Li & Changwei Zhang & Yinzi Li & Guanwei Wu & Xilin Hou & Xueping Zhou & Aiming Wang, 2018. "Beclin1 restricts RNA virus infection in plants through suppression and degradation of the viral polymerase," Nature Communications, Nature, vol. 9(1), pages 1-17, 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. 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.
    2. 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.
    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. 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.
    6. 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.
    7. 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.
    8. 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.
    9. 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.
    10. 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.
    11. 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.
    12. 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.
    13. 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.
    14. 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.
    15. 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.
    16. 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.
    17. 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.
    18. 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.
    19. 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.
    20. Qi Li & Mingxi Zhou & Shweta Chhajed & Fahong Yu & Sixue Chen & Yanping Zhang & Zhonglin Mou, 2023. "N-hydroxypipecolic acid triggers systemic acquired resistance through extracellular NAD(P)," Nature Communications, Nature, vol. 14(1), pages 1-17, 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:14:y:2023:i:1:d:10.1038_s41467-023-39426-0. 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.