IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v16y2025i1d10.1038_s41467-025-62326-4.html
   My bibliography  Save this article

A fungal effector promotes infection via stabilizing a negative regulatory factor of chloroplast immunity

Author

Listed:
  • Kunqin Xiao

    (Jilin University)

  • Feng Yang

    (Jilin University
    Northwest A&F University)

  • Wenjing Cui

    (Jilin University)

  • Anmo Li

    (Jilin University)

  • Jeffrey A. Rollins

    (University of Florida)

  • Jinxin Guo

    (Jilin University)

  • Xinhua Sun

    (Southwest University)

  • Fengting Wang

    (Jilin University)

  • Xiaojie Wang

    (Northwest A&F University)

  • Xun Xu

    (Jilin University)

  • Yanhua Zhang

    (Jilin University)

  • Xianghui Zhang

    (Jilin University)

  • Jinliang Liu

    (Jilin University)

  • Hongyu Pan

    (Jilin University)

Abstract

Chloroplasts are crucial players in immunity and photosynthesis. However, how chloroplasts arrange the transition between photosynthesis and immunity and how pathogens manipulate this transition remains elusive. Here we report an effector SsCm1 from Sclerotinia sclerotiorum, one of devastating phytopathogenic fungi, inhibits chloroplast immunity and resistance to pathogens, and alleviates photoinhibition in immune state. This is accomplished through stabilizing the conserved chloroplast protein MORF2, which is degraded during immunization and is a suppressor of photoinhibition, cell death, and chloroplast immunity. Overexpression of SsCm1 or MORF2 in plants represses basic immunity and resistance to pathogens, whereas deletion of SsCm1 reduces S. sclerotiorum virulence. Notably, SsCm1 possesses no chorismate mutase activity, which is different from the previously reported Cm effectors. This work reveals a strategy to fine-tune growth-defense balance in chloroplasts by manipulating MORF2, and a pathogenic strategy to subvert the process and promote infection via enzymatically nonfunctional effector stabilizing MORF2.

Suggested Citation

  • Kunqin Xiao & Feng Yang & Wenjing Cui & Anmo Li & Jeffrey A. Rollins & Jinxin Guo & Xinhua Sun & Fengting Wang & Xiaojie Wang & Xun Xu & Yanhua Zhang & Xianghui Zhang & Jinliang Liu & Hongyu Pan, 2025. "A fungal effector promotes infection via stabilizing a negative regulatory factor of chloroplast immunity," Nature Communications, Nature, vol. 16(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-62326-4
    DOI: 10.1038/s41467-025-62326-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-025-62326-4
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-025-62326-4?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. Armin Djamei & Kerstin Schipper & Franziska Rabe & Anupama Ghosh & Volker Vincon & Jörg Kahnt & Sonia Osorio & Takayuki Tohge & Alisdair R. Fernie & Ivo Feussner & Kirstin Feussner & Peter Meinicke & , 2011. "Metabolic priming by a secreted fungal effector," Nature, Nature, vol. 478(7369), pages 395-398, October.
    2. 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.
    3. Hailong Guo & Peiqiang Feng & Wei Chi & Xuwu Sun & Xiumei Xu & Yuan Li & Dongtao Ren & Congming Lu & Jean David Rochaix & Dario Leister & Lixin Zhang, 2016. "Plastid-nucleus communication involves calcium-modulated MAPK signalling," Nature Communications, Nature, vol. 7(1), pages 1-15, November.
    4. 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.
    5. Hironari Nomura & Teiko Komori & Shuhei Uemura & Yui Kanda & Koji Shimotani & Kana Nakai & Takuya Furuichi & Kohsuke Takebayashi & Takanori Sugimoto & Satoshi Sano & I Nengah Suwastika & Eiichiro Fuku, 2012. "Chloroplast-mediated activation of plant immune signalling in Arabidopsis," Nature Communications, Nature, vol. 3(1), pages 1-11, January.
    6. Jie Wu & Yue Wang & Haodong Chen & Tongda Xu & Wenqiang Yang & Xiaofeng Fang, 2025. "Solid-like condensation of MORF8 inhibits RNA editing under heat stress in Arabidopsis," Nature Communications, Nature, vol. 16(1), pages 1-13, December.
    7. Qiang Xu & Chunlei Tang & Xiaodong Wang & Shutian Sun & Jinren Zhao & Zhensheng Kang & Xiaojie Wang, 2019. "An effector protein of the wheat stripe rust fungus targets chloroplasts and suppresses chloroplast function," Nature Communications, Nature, vol. 10(1), pages 1-13, 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. 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.
    2. Zhiyi Chen & Jianhua Huang & Jianyu Li & Frank L. H. Menke & Jonathan D. G. Jones & Hailong Guo, 2025. "Reversible ubiquitination conferred by domain shuffling controls paired NLR immune receptor complex homeostasis in plant immunity," Nature Communications, Nature, vol. 16(1), pages 1-15, December.
    3. Qiuhua Yang & Zhuowen Li & Kaixiang Guan & Zhenghong Wang & Xianli Tang & Yechun Hong & Zhijian Liu & Jixian Zhai & Ancheng Huang & Yanping Long & Yi Song, 2025. "Comparative single-nucleus RNA-seq analysis revealed localized and cell type-specific pathways governing root-microbiome interactions," Nature Communications, Nature, vol. 16(1), pages 1-16, December.
    4. Sayaka Matsui & Saki Noda & Keiko Kuwata & Mika Nomoto & Yasuomi Tada & Hidefumi Shinohara & Yoshikatsu Matsubayashi, 2024. "Arabidopsis SBT5.2 and SBT1.7 subtilases mediate C-terminal cleavage of flg22 epitope from bacterial flagellin," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    5. Ci Kong & Yin Yang & Tiancong Qi & Shuyi Zhang, 2025. "Predictive genetic circuit design for phenotype reprogramming in plants," Nature Communications, Nature, vol. 16(1), pages 1-14, December.
    6. Mengmeng Li & Zige Yang & Cheng Chang, 2022. "Susceptibility Is New Resistance: Wheat Susceptibility Genes and Exploitation in Resistance Breeding," Agriculture, MDPI, vol. 12(9), pages 1-13, September.
    7. Tianyiyi He & Jinge Wang & Donghui Hu & Yanqin Yang & Eunyoung Chae & Chengkuo Lee, 2025. "Epidermal electronic-tattoo for plant immune response monitoring," Nature Communications, Nature, vol. 16(1), pages 1-14, December.
    8. Yue Li & Xiangru Qu & Wenjuan Yang & Qin Wu & Xiaodong Wang & Qiantao Jiang & Jian Ma & Yazhou Zhang & Pengfei Qi & Guoyue Chen & Youliang Zheng & Xiaojie Wang & Yuming Wei & Qiang Xu, 2025. "A fungal pathogen suppresses host leaf senescence to increase infection," Nature Communications, Nature, vol. 16(1), pages 1-15, December.
    9. Fabien Lonjon & Yan Lai & Nasrin Askari & Niharikaa Aiyar & Cedoljub Bundalovic-Torma & Bradley Laflamme & Pauline W. Wang & Darrell Desveaux & David S. Guttman, 2024. "The effector-triggered immunity landscape of tomato against Pseudomonas syringae," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    10. 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.
    11. 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.
    12. 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.
    13. 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.
    14. Li Fan & Katja Fröhlich & Eric Melzer & Rory N. Pruitt & Isabell Albert & Lisha Zhang & Anna Joe & Chenlei Hua & Yanyue Song & Markus Albert & Sang-Tae Kim & Detlef Weigel & Cyril Zipfel & Eunyoung Ch, 2022. "Genotyping-by-sequencing-based identification of Arabidopsis pattern recognition receptor RLP32 recognizing proteobacterial translation initiation factor IF1," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    15. Xia Yang & Leilei Zhang & Jiajie Wei & Lexin Liu & Di Liu & Xiangning Yan & Minjie Yuan & Lingran Zhang & Ning Zhang & Yan Ren & Feng Chen, 2025. "A TaSnRK1α-TaCAT2 model mediates resistance to Fusarium crown rot by scavenging ROS in common wheat," Nature Communications, Nature, vol. 16(1), pages 1-15, December.
    16. Muhammad Awais Zahid & Nam Phuong Kieu & Frida Meijer Carlsen & Marit Lenman & Naga Charan Konakalla & Huanjie Yang & Sunmoon Jyakhwa & Jozef Mravec & Ramesh Vetukuri & Bent Larsen Petersen & Svante R, 2024. "Enhanced stress resilience in potato by deletion of Parakletos," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    17. Xiaofan Liu & Huihui Zhao & Mingyun Yuan & Pengyue Li & Jiatao Xie & Yanping Fu & Bo Li & Xiao Yu & Tao Chen & Yang Lin & Weidong Chen & Daohong Jiang & Jiasen Cheng, 2024. "An effector essential for virulence of necrotrophic fungi targets plant HIRs to inhibit host immunity," Nature Communications, Nature, vol. 15(1), pages 1-16, 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:16:y:2025:i:1:d:10.1038_s41467-025-62326-4. 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.