J Integr Plant Biol ›› 2025, Vol. 67 ›› Issue (1): 150-168.DOI: 10.1111/jipb.13800  cstr: 32098.14.jipb.13800

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  • 收稿日期:2024-07-10 接受日期:2024-10-09 出版日期:2025-01-01 发布日期:2024-10-31

Recognition of a salivary effector by the TNL protein RCSP promotes effector-triggered immunity and systemic resistance in Nicotiana benthamiana

Weiwei Rao1†, Tingting Ma1†, Jiayuan Cao1, Yajun Zhang1, Sisi Chen1, Shu Lin1, Xiaoxiao Liu1, Guangcun He2 and Li Wan1,3*   

  1. 1. Key Laboratory of Plant Design, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai 200032, China
    2. National Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan 430072, China
    3. University of Chinese Academy of Sciences, Beijing 100049, China
    †These authors contributed equally to this work.
    *Correspondence: Li Wan (lwan@cemps.ac.cn)
  • Received:2024-07-10 Accepted:2024-10-09 Online:2025-01-01 Published:2024-10-31
  • Supported by:
    This work was supported by the Key Laboratory of Plant Design, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences (Li Wan), National Natural Science Foundation of China 32270304 (Li Wan), and Chinese Academy of Sciences Strategic Priority Research Program Type‐B XDB27040214 (Li Wan).

Abstract: Insects secret chemosensory proteins (CSPs) into plant cells as potential effector proteins during feeding. The molecular mechanisms underlying how CSPs activate plant immunity remain largely unknown. We show that CSPs from six distinct insect orders induce dwarfism when overexpressed in Nicotiana benthamiana. Agrobacterium-mediated transient expression of Nilaparvata lugens CSP11 (NlCSP11) triggered cell death and plant dwarfism, both of which were dependent on ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1), N requirement gene 1 (NRG1) and SENESCENCE-ASSOCIATED GENE 101 (SAG101), indicating the activation of effector-triggered immunity (ETI) in N. benthamiana. Overexpression of NlCSP11 led to stronger systemic resistance against Pseudomonas syringae DC3000 lacking effector HopQ1-1 and tobacco mosaic virus, and induced higher accumulation of salicylic acid (SA) in uninfiltrated leaves compared to another effector XopQ that is recognized by a Toll-interleukin-1 receptor (TIR) domain nucleotide-binding leucine-rich repeat receptor (TNL) called ROQ1 in N. benthamiana. Consistently, NlCSP11-induced dwarfism and systemic resistance, but not cell death, were abolished in N. benthamiana transgenic line expressing the SA-degrading enzyme NahG. Through large-scale virus-induced gene silencing screening, we identified a TNL protein that mediates the recognition of CSPs (RCSP), including aphid effector MP10 that triggers resistance against aphids in N. benthamiana. Co-immunoprecipitation, bimolecular fluorescence complementation and AlphaFold2 prediction unveiled an interaction between NlCSP11 and RCSP. Interestingly, RCSP does not contain the conserved catalytic glutamic acid in the TIR domain, which is required for TNL function. Our findings point to enhanced ETI and systemic resistance by a TNL protein via hyperactivation of the SA pathway. Moreover, RCSP is the first TNL identified to recognize an insect effector.

Key words: chemosensory protein, effector, effector‐triggered immunity, salicylic acid, TIR‐NBS‐LRR

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