Cytoplasmic and nuclear Sw-5b NLR act both independently and synergistically to dictate full host defense against tospovirus infection

• Published in: bioRxiv
• Main Authors: Chen, Hongyu, Qian, Xin, Chen, Xiaojiao, Yang, Tongqing, Feng, Mingfeng, Chen, Jing, Cheng, Ruixiang, Hong, Hao, Zheng, Ying, Mei, Yuzhen, Shen, Danyu, Xu, Yi, Zhu, Min, Ding, Xin Shun, Tao, Xiaorong
• Format: Paper
• Language: English
• Published: Cold Spring Harbor Cold Spring Harbor Laboratory Press 05.02.2021
• Subjects: Apoptosis; Cell death; Cytoplasm; Defense; Disseminated infection; Host plants; Infections; Innate immunity; Intracellular; Leucine; Localization; Pathogens; Replication; Roles; Viruses; Wilt
• DOI: 10.1101/2020.12.24.424293

Summary * Plant intracellular nucleotide binding-leucine-rich repeat (NLR) receptors play critical roles in mediating host immunity to pathogen attack. We use tomato Sw-5b::tospovirus as a model system to study the specific role of the compartmentalized plant NLR in dictating host defense against virus at different infection steps. * We demonstrated here that tomato NLR Sw-5b translocates to cytoplasm and nucleus, respectively, to play different roles in inducing host resistances against Tomato spotted wilt tospovirus (TSWV) infection. The cytoplasmic Sw-5b functions to induce a strong cell death response to inhibit TSWV replication. This host response is, however, insufficient to block viral intercellular and long-distance movement. The nucleus-localized Sw-5b triggers a host defense that weakly inhibits viral replication but strongly impedes virus intercellular and systemic movement. Furthermore, the cytoplasmic and nuclear Sw-5b act synergistically to dictate full host defense to TSWV infection. * We further demonstrated that the extended N-terminal Solanaceae domain (SD) of Sw-5b plays critical roles in cytoplasm/nucleus partitioning. Sw-5b nucleotide-binding leucine-rich repeat (NB-LRR) controls its cytoplasm localization. Strikingly, the SD but not coil-coil (CC) domain is crucial for Sw-5b receptor to translocate from cytoplasm to nucleus to trigger the immunity. The SD was found to interact with importins. Silencing both importin α and β expression disrupted Sw-5b nucleus translocation and host immunity against TSWV systemic infection. * Collectively, our findings suggest that Sw-5b bifurcates disease resistances by cytoplasm/nucleus partitioning to block different infection steps of TSWV. The findings also identified a new regulatory role of extra domain of a plant NLR in mediating host innate immunity. Competing Interest Statement The authors have declared no competing interest. Footnotes * Plant intracellular nucleotide binding-leucine-rich repeat (NLR) receptors play critical roles in mediating host immunity to pathogen attack. Successful virus infection in plant involves several essential steps including viral replication, intercellular and long-distance movement. How plant NLRs induce resistances against virus infection remains largely unknown. We demonstrated here that tomato NLR Sw-5b locates to cytoplasm and nucleus, respectively, to play different roles in inducing host resistances against tospovirus infection. The cytoplasmic Sw-5b functions to induce a strong cell death response to inhibit TSWV replication. This host response is, however, insufficient to block viral intercellular and long-distance movement. The nucleus-localized Sw-5b triggers a host defense that weakly inhibit viral replication but strongly impede virus intercellular and systemic movement. Furthermore, the cytoplasmic and nuclear Sw-5b act synergistically to confer a strong immunity to TSWV infection. Our finding adds a new knowledge to our current understanding on the plant NLRs-triggered immunity against virus infection.