IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-29788-2.html
   My bibliography  Save this article

A fungal extracellular effector inactivates plant polygalacturonase-inhibiting protein

Author

Listed:
  • Wei Wei

    (Washington State University)

  • Liangsheng Xu

    (Northwestern A&F University)

  • Hao Peng

    (Washington State University)

  • Wenjun Zhu

    (Wuhan Polytechnic University)

  • Kiwamu Tanaka

    (Washington State University
    Washington State University)

  • Jiasen Cheng

    (Huazhong Agricultural University)

  • Karen A. Sanguinet

    (Washington State University
    Washington State University)

  • George Vandemark

    (Washington State University
    Grain Legume Genetics and Physiology Research Unit)

  • Weidong Chen

    (Washington State University
    Washington State University
    Washington State University
    Grain Legume Genetics and Physiology Research Unit)

Abstract

Plant pathogens degrade cell wall through secreted polygalacturonases (PGs) during infection. Plants counteract the PGs by producing PG-inhibiting proteins (PGIPs) for protection, reversibly binding fungal PGs, and mitigating their hydrolytic activities. To date, how fungal pathogens specifically overcome PGIP inhibition is unknown. Here, we report an effector, Sclerotinia sclerotiorum PGIP-INactivating Effector 1 (SsPINE1), which directly interacts with and functionally inactivates PGIP. S. sclerotiorum is a necrotrophic fungus that causes stem rot diseases on more than 600 plant species with tissue maceration being the most prominent symptom. SsPINE1 enhances S. sclerotiorum necrotrophic virulence by specifically interacting with host PGIPs to negate their polygalacturonase-inhibiting function via enhanced dissociation of PGIPs from PGs. Targeted deletion of SsPINE1 reduces the fungal virulence. Ectopic expression of SsPINE1 in plant reduces its resistance against S. sclerotiorum. Functional and genomic analyses reveal a conserved virulence mechanism of cognate PINE1 proteins in broad host range necrotrophic fungal pathogens.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29788-2
    DOI: 10.1038/s41467-022-29788-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-29788-2
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-29788-2?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. Jonathan D. G. Jones & Jeffery L. Dangl, 2006. "The plant immune system," Nature, Nature, vol. 444(7117), pages 323-329, November.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Wen Li & Peng Li & Yizhen Deng & Junjian Situ & Zhuoyuan He & Wenzhe Zhou & Minhui Li & Pinggen Xi & Xiangxiu Liang & Guanghui Kong & Zide Jiang, 2024. "A plant cell death-inducing protein from litchi interacts with Peronophythora litchii pectate lyase and enhances plant resistance," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

    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. Rongrong Zhang & Yu Wu & Xiangru Qu & Wenjuan Yang & Qin Wu & Lin Huang & Qiantao Jiang & Jian Ma & Yazhou Zhang & Pengfei Qi & Guoyue Chen & Yunfeng Jiang & Youliang Zheng & Xiaojie Wang & Yuming Wei, 2024. "The RING-finger ubiquitin E3 ligase TaPIR1 targets TaHRP1 for degradation to suppress chloroplast function," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    8. 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.
    9. 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.
    10. 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.
    11. Shen Huang & Chunli Wang & Zixuan Ding & Yaqian Zhao & Jing Dai & Jia Li & Haining Huang & Tongkai Wang & Min Zhu & Mingfeng Feng & Yinghua Ji & Zhongkai Zhang & Xiaorong Tao, 2024. "A plant NLR receptor employs ABA central regulator PP2C-SnRK2 to activate antiviral immunity," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    12. 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.
    13. Conner J. Rogan & Yin-Yuin Pang & Sophie D. Mathews & Sydney E. Turner & Alexandra J. Weisberg & Silke Lehmann & Doris Rentsch & Jeffrey C. Anderson, 2024. "Transporter-mediated depletion of extracellular proline directly contributes to plant pattern-triggered immunity against a bacterial pathogen," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    14. 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.
    15. 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.
    16. 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.
    17. 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.
    18. 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.
    19. 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.
    20. 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.

    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:13:y:2022:i:1:d:10.1038_s41467-022-29788-2. 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.