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Pattern-recognition receptors are required for NLR-mediated plant immunity

Author

Listed:
  • Minhang Yuan

    (Institute of Plant Physiology and Ecology, Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Zeyu Jiang

    (Institute of Plant Physiology and Ecology, Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Guozhi Bi

    (Institute of Genetics and Developmental Biology, Innovation Academy for Seed Design, Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Kinya Nomura

    (Michigan State University)

  • Menghui Liu

    (Henan University)

  • Yiping Wang

    (Institute of Plant Physiology and Ecology, Chinese Academy of Sciences)

  • Boying Cai

    (Institute of Plant Physiology and Ecology, Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Jian-Min Zhou

    (Institute of Genetics and Developmental Biology, Innovation Academy for Seed Design, Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Sheng Yang He

    (Michigan State University
    Duke University
    Duke University)

  • Xiu-Fang Xin

    (Institute of Plant Physiology and Ecology, Chinese Academy of Sciences
    University of Chinese Academy of Sciences
    Institute of Plant Physiology and Ecology, Chinese Academy of Sciences)

Abstract

The plant immune system is fundamental for plant survival in natural ecosystems and for productivity in crop fields. Substantial evidence supports the prevailing notion that plants possess a two-tiered innate immune system, called pattern-triggered immunity (PTI) and effector-triggered immunity (ETI). PTI is triggered by microbial patterns via cell surface-localized pattern-recognition receptors (PRRs), whereas ETI is activated by pathogen effector proteins via predominantly intracellularly localized receptors called nucleotide-binding, leucine-rich repeat receptors (NLRs)1–4. PTI and ETI are initiated by distinct activation mechanisms and involve different early signalling cascades5,6. Here we show that Arabidopsis PRR and PRR co-receptor mutants—fls2 efr cerk1 and bak1 bkk1 cerk1 triple mutants—are markedly impaired in ETI responses when challenged with incompatible Pseudomonas syrinage bacteria. We further show that the production of reactive oxygen species by the NADPH oxidase RBOHD is a critical early signalling event connecting PRR- and NLR-mediated immunity, and that the receptor-like cytoplasmic kinase BIK1 is necessary for full activation of RBOHD, gene expression and bacterial resistance during ETI. Moreover, NLR signalling rapidly augments the transcript and/or protein levels of key PTI components. Our study supports a revised model in which potentiation of PTI is an indispensable component of ETI during bacterial infection. This revised model conceptually unites two major immune signalling cascades in plants and mechanistically explains some of the long-observed similarities in downstream defence outputs between PTI and ETI.

Suggested Citation

  • Minhang Yuan & Zeyu Jiang & Guozhi Bi & Kinya Nomura & Menghui Liu & Yiping Wang & Boying Cai & Jian-Min Zhou & Sheng Yang He & Xiu-Fang Xin, 2021. "Pattern-recognition receptors are required for NLR-mediated plant immunity," Nature, Nature, vol. 592(7852), pages 105-109, April.
  • Handle: RePEc:nat:nature:v:592:y:2021:i:7852:d:10.1038_s41586-021-03316-6
    DOI: 10.1038/s41586-021-03316-6
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    Citations

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    Cited by:

    1. 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.
    2. Md Mijanur Rahman Rajib & Kuikui Li & Md Saikat Hossain Bhuiyan & Wenxia Wang & Jin Gao & Heng Yin, 2024. "Konjac Glucomannan Oligosaccharides (KGMOS) Confers Innate Immunity against Phytophthora nicotianae in Tobacco," Agriculture, MDPI, vol. 14(8), pages 1-17, August.
    3. 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.
    4. 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.
    5. 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.
    6. Gengshen Chen & Bao Zhang & Junqiang Ding & Hongze Wang & Ce Deng & Jiali Wang & Qianhui Yang & Qianyu Pi & Ruyang Zhang & Haoyu Zhai & Junfei Dong & Junshi Huang & Jiabao Hou & Junhua Wu & Jiamin Que, 2022. "Cloning southern corn rust resistant gene RppK and its cognate gene AvrRppK from Puccinia polysora," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    7. Mervin Chun-Yi Ang & Jolly Madathiparambil Saju & Thomas K. Porter & Sayyid Mohaideen & Sreelatha Sarangapani & Duc Thinh Khong & Song Wang & Jianqiao Cui & Suh In Loh & Gajendra Pratap Singh & Nam-Ha, 2024. "Decoding early stress signaling waves in living plants using nanosensor multiplexing," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    8. 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.

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