Cavity surface residues of PAD4 and SAG101 contribute to EDS1 dimer signaling specificity in plant immunity
Dongus, Joram A. | Bhandari, Deepak D. | Penner, Eva | Lapin, Dmitry | Stolze, Sara C. | Harzen, Anne | Patel, Monika | Archer, Lani | Dijkgraaf, Lucas | Shah, Jyoti | Nakagami, Hirofumi | Parker, Jane E.
Arabidopsis pathogen effector‐triggered immunity (ETI) is controlled by a family of three lipase‐like proteins (EDS1, PAD4, and SAG101) and two subfamilies of HET‐S/LOB‐B (HeLo)‐domain “helper” nucleotide‐binding/leucine‐rich repeats (ADR1s and NRG1s). EDS1‐PAD4 dimers cooperate with ADR1s, and EDS1‐SAG101 dimers with NRG1s, in two separate defense‐promoting modules. EDS1‐PAD4‐ADR1 and EDS1‐SAG101‐NRG1 complexes were detected in immune‐activated leaf extracts but the molecular determinants for specific complex formation and function remain unknown. EDS1 signaling is mediated by a C‐terminal EP domain (EPD) surface surrounding a cavity formed by the heterodimer. Here we investigated whether the EPDs of PAD4 and SAG101 contribute to EDS1 dimer functions. Using a structure‐guided approach, we undertook a comprehensive mutational analysis of Arabidopsis PAD4. We identify two conserved residues (Arg314 and Lys380) lining the PAD4 EPD cavity that are essential for EDS1‐PAD4–mediated pathogen resistance, but are dispensable for the PAD4‐mediated restriction of green peach aphid infestation. Positionally equivalent Met304 and Arg373 at the SAG101 EPD cavity are required for EDS1‐SAG101 promotion of ETI‐related cell death. In a PAD4 and SAG101 interactome analysis of ETI‐activated tissues, PAD4ᴿ³¹⁴ᴬ and SAG101ᴹ³⁰⁴ᴿ EPD variants maintain interaction with EDS1 but lose association, respectively, with helper nucleotide‐binding/leucine‐rich repeats ADR1‐L1 and NRG1.1, and other immune‐related proteins. Our data reveal a fundamental contribution of similar but non‐identical PAD4 and SAG101 EPD surfaces to specific EDS1 dimer protein interactions and pathogen immunity.
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