The NLR immune receptor ADR1 and lipase-like proteins EDS1 and PAD4 mediate stomatal immunity in Nicotiana benthamiana and Arabidopsis

• Published in: The Plant cell 2024-01, Vol.36 (2), p.427-446
• Main Authors: Wang, Hanling, Song, Susheng, Gao, Shang, Yu, Qiangsheng, Zhang, Haibo, Cui, Xiulin, Fan, Jun, Xin, Xiufang, Liu, Yule, Staskawicz, Brian, Qi, Tiancong
• Format: Article
• Language: English
• Subjects: Arabidopsis - metabolism; Arabidopsis Proteins - metabolism; Carboxylic Ester Hydrolases - genetics; DNA-Binding Proteins - metabolism; Lipase - metabolism; Nicotiana - genetics; Plant Diseases - microbiology; Plant Immunity - genetics
• ISSN: 1040-4651; 1532-298X; 1532-298X
• DOI: 10.1093/plcell/koad270

Abstract In the presence of pathogenic bacteria, plants close their stomata to prevent pathogen entry. Intracellular nucleotide-binding leucine-rich repeat (NLR) immune receptors recognize pathogenic effectors and activate effector-triggered immune responses. However, the regulatory and molecular mechanisms of stomatal immunity involving NLR immune receptors are unknown. Here, we show that the Nicotiana benthamiana RPW8-NLR central immune receptor ACTIVATED DISEASE RESISTANCE 1 (NbADR1), together with the key immune proteins ENHANCED DISEASE SUSCEPTIBILITY 1 (NbEDS1) and PHYTOALEXIN DEFICIENT 4 (NbPAD4), plays an essential role in bacterial pathogen- and flg22-induced stomatal immunity by regulating the expression of salicylic acid (SA) and abscisic acid (ABA) biosynthesis or response-related genes. NbADR1 recruits NbEDS1 and NbPAD4 in stomata to form a stomatal immune response complex. The transcription factor NbWRKY40e, in association with NbEDS1 and NbPAD4, modulates the expression of SA and ABA biosynthesis or response-related genes to influence stomatal immunity. NbADR1, NbEDS1, and NbPAD4 are required for the pathogen infection-enhanced binding of NbWRKY40e to the ISOCHORISMATE SYNTHASE 1 promoter. Moreover, the ADR1-EDS1-PAD4 module regulates stomatal immunity in Arabidopsis (Arabidopsis thaliana). Collectively, our findings show the pivotal role of the core intracellular immune receptor module ADR1-EDS1-PAD4 in stomatal immunity, which enables plants to limit pathogen entry. Intracellular receptor NbADR1 forms a module with immunity proteins NbEDS1 and NbPAD4, functioning together with transcription factor NbWRKY40e to mediate stomatal immunity in Nicotiana benthamiana.