The NLR immune receptor ADR1 and lipase-like proteins EDS1 and PAD4 mediate stomatal immunity

Hanling Wang, Susheng Song, Shang Gao, Qiangsheng Yu, Haibo Zhang, Xiulin Cui, Jun Fan, Xiufang Xin, Yule Liu, Brian Staskawicz, Tiancong Qi
Center for Plant Biology, School of Life Sciences, Tsinghua University, Beijing 100084, China.

In the presence of pathogenic bacteria, plants close their stomata to prevent pathogen entry. Intracellular NLR immune receptors recognize pathogenic effectors and activate effector-triggered immune responses. However, the regulatory and molecular mechanisms of stomatal immunity by NLR immune receptors are unknown. Here, we show that the Nicotiana benthamiana RPW8-NLR central immune receptor NbADR1, together with the key immune proteins NbEDS1 and NbPAD4, plays an essential role in bacterial pathogen- and flg22-induced stomatal immunity via salicylic acid (SA) and abscisic acid (ABA) pathways. NbADR1 recruits NbEDS1/NbPAD4 in stomata to form a stomatal immune response complex. The transcription factor NbWRKY40e, in association with NbEDS1/NbPAD4, contributes to stomatal immunity by modulating SA and ABA pathways. Nb ADR1, Nb EDS1, and Nb PAD4 are required for the pathogen infection-enhanced binding of NbWRKY40e to the ICS1 promoter. Moreover, the ADR1-EDS1-PAD4 module regulates stomatal immunity in Arabidopsis. 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.