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

作　　者：Weiwei Rao Tingting Ma Jiayuan Cao Yajun Zhang Sisi Chen Shu Lin Xiaoxiao Liu Guangcun He Li Wan 

机构地区：[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

出　　处：《Journal of Integrative Plant Biology》2025年第1期150-168,共19页植物学报(英文版)

基　　金：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);Chinese Academy of Sciences Strategic Priority Research Program Type-B XDB27040214(Li Wan)。

摘　　要：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 gene1(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 Tollinterleukin-1 receptor(TIR)domain nucleotidebinding 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 Nah G.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.Coimmunoprecipitation,bimolecular fluorescence complementation and Alpha Fold2 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.

关 键 词：chemosensory protein EFFECTOR effector-triggered immunity salicylic acid TIR-NBS-LRR 

分 类 号：R73[医药卫生—肿瘤]