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bioRxiv · 10.1101/2024.10.29.620780

Switch of TIR signaling by a Ca2+ sensor activates ADR1 recognition of pRib-AMP-EDS1-PAD4 for stomatal immunity

Wang, H.·Tan, J.·Cui, X.·Bai, Y.·Gao, S.·Staskawicz, B.·Song, S.·Yan, C.·Qi, T.
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Abstract

Plants swiftly close stomata upon detecting pathogen entry, a crucial defense termed stomatal immunity. The process is initiated by cell-surface pattern recognition receptors (PRRs) that perceive pathogen-associated molecular patterns (PAMPs) and evoke a series of early cellular responses including calcium ions (Ca2+) influx, and is conducted by the intracellular nucleotide-binding leucine-rich-repeat receptors (NLRs) ADR1s within an EDS1-PAD4-ADR1 module. However, the underlying mechanisms linking PRR signaling to the NLRs ADR1s remain unclear. Here, we show that the Nicotiana benthamiana Toll/interleukin-1 receptor (TIR)-only protein Stomatal TIR1 (STIR1) produces the immune molecule pRib-AMP, induces formation of EDS1-PAD4-ADR1 complexes, and mediates stomatal immunity. The Inhibitor of Stomatal Immunity C2-domain protein 1 (ISIC1) interacts with and constrains STIR1 function at basal condition, whereas upon pathogen infection, ISIC1 senses Ca2+ signals and de-represses STIR1 signaling. Cryo-electron microscopy structure of pathogen infection-elicited Arabidopsis AtEDS1-AtPAD4-AtADR1-L2 complex reveals the pRib-AMP binding to AtEDS1-AtPAD4 receptor and the AtADR1-L2 recognition of pRib-AMP-AtPAD4-AtEDS1 for stomatal immunity. Collectively, this study uncovers a repression/de-repression mechanism linking PRR signaling to NLRs by a Ca2+ sensor/TIR-only node, and elucidates an NLR recognition mechanism of the pRib-AMP-EDS1-PAD4 complex in governing innate immunity. SynopsisAt basal condition, the Ca2+ sensor ISIC1 interacts with and inhibits the TIR-only protein STIR1; upon pathogen infection, ISIC1 perceives Ca2+ signal and releases STIR1 to produce pRib-AMP; the EDS1-PAD4 receptor binds pRib-AMP and is recognized by the NLR ADR1-L2, thereby activating stomatal immunity.

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Wang, H., Tan, J., Cui, X., Bai, Y., Gao, S., Staskawicz, B., Song, S., Yan, C., Qi, T.. 2024-11-02. Switch of TIR signaling by a Ca2+ sensor activates ADR1 recognition of pRib-AMP-EDS1-PAD4 for stomatal immunity. https://doi.org/10.1101/2024.10.29.620780

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