NLR surveillance of pathogen interference with hormone receptors induces immunity

Jing Chen, Yanxiao Zhao, Xuanjie Luo, Hao Hong, Tongqing Yang, Shen Huang, Chunli Wang, Hongyu Chen, Xin Qian, Mingfeng Feng, Zhengqiang Chen, Yongxin Dong, Zhenchuan Ma, Jia Li, Min Zhu, Sheng Yang He, Savithramma P. Dinesh-Kumar and Xiaorong Tao ()
Additional contact information
Jing Chen: Nanjing Agricultural University
Yanxiao Zhao: Nanjing Agricultural University
Xuanjie Luo: Nanjing Agricultural University
Hao Hong: Nanjing Agricultural University
Tongqing Yang: Nanjing Agricultural University
Shen Huang: Nanjing Agricultural University
Chunli Wang: Nanjing Agricultural University
Hongyu Chen: Nanjing Agricultural University
Xin Qian: Nanjing Agricultural University
Mingfeng Feng: Nanjing Agricultural University
Zhengqiang Chen: Nanjing Agricultural University
Yongxin Dong: Nanjing Agricultural University
Zhenchuan Ma: Nanjing Agricultural University
Jia Li: Nanjing Agricultural University
Min Zhu: Nanjing Agricultural University
Sheng Yang He: Duke University
Savithramma P. Dinesh-Kumar: University of California
Xiaorong Tao: Nanjing Agricultural University

Nature, 2023, vol. 613, issue 7942, 145-152

Abstract: Abstract Phytohormone signalling pathways have an important role in defence against pathogens mediated by cell-surface pattern recognition receptors and intracellular nucleotide-binding leucine-rich repeat class immune receptors1,2 (NLR). Pathogens have evolved counter-defence strategies to manipulate phytohormone signalling pathways to dampen immunity and promote virulence3. However, little is known about the surveillance of pathogen interference of phytohormone signalling by the plant innate immune system. The pepper (Capsicum chinense) NLR Tsw, which recognizes the effector nonstructural protein NSs encoded by tomato spotted wilt orthotospovirus (TSWV), contains an unusually large leucine-rich repeat (LRR) domain. Structural modelling predicts similarity between the LRR domain of Tsw and those of the jasmonic acid receptor COI1, the auxin receptor TIR1 and the strigolactone receptor partner MAX2. This suggested that NSs could directly target hormone receptor signalling to promote infection, and that Tsw has evolved a LRR resembling those of phytohormone receptors LRR to induce immunity. Here we show that NSs associates with COI1, TIR1 and MAX2 through a common repressor—TCP21—which interacts directly with these phytohormone receptors. NSs enhances the interaction of COI1, TIR1 or MAX2 with TCP21 and blocks the degradation of corresponding transcriptional repressors to disable phytohormone-mediated host immunity to the virus. Tsw also interacts directly with TCP21 and this interaction is enhanced by viral NSs. Downregulation of TCP21 compromised Tsw-mediated defence against TSWV. Together, our findings reveal that a pathogen effector targets TCP21 to inhibit phytohormone receptor function, promoting virulence, and a plant NLR protein has evolved to recognize this interference as a counter-virulence strategy, thereby activating immunity.

Date: 2023
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DOI: 10.1038/s41586-022-05529-9

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