A coevolved EDS1-SAG101-NRG1 module mediates cell death signaling by TIR-domain immune receptors

Dmitry Lapin, Viera Kovacova, Xinhua Sun, Joram Dongus, Deepak Bhandari, Patrick von Born, Jaqueline Bautor, Nina Guarneri, Jakub Rzemieniewski, Johannes Stuttmann, Andreas Beyer, Jane E. Parker*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

33 Citations (Scopus)

Abstract

Plant intracellular nucleotide-binding/leucine-rich repeat (NLR) immune receptors are activated by pathogen effectors to trigger host defenses and cell death. Toll-Interleukin1-receptor (TIR)-domain NLRs (TNLs) converge on the Enhanced Disease Susceptibility1 (EDS1) family of lipase-like proteins for all resistance outputs. In Arabidopsis TNL immunity, AtEDS1 heterodimers with Phytoalexin Deficient4 (AtPAD4) transcriptionally boost basal defense pathways. AtEDS1 uses the same surface to interact with PAD4-related Senescence-Associated Gene101 (AtSAG101), but the role of AtEDS1-AtSAG101 heterodimers was unclear. We show that AtEDS1-AtSAG101 function together with AtNRG1 coiled-coil domain helper NLRs as a coevolved TNL cell death signaling module. AtEDS1-AtSAG101-AtNRG1 cell death activity is transferable to the solanaceous species, Nicotiana benthamiana, and cannot be substituted by AtEDS1-AtPAD4 with AtNRG1 or AtEDS1-AtSAG101 with endogenous NbNRG1. Analysis of EDS1-family evolutionary rate variation and heterodimer structure-guided phenotyping of AtEDS1 variants or AtPAD4-AtSAG101 chimeras identify closely aligned ɑ-helical coil surfaces in the AtEDS1-AtSAG101 partner C-terminal domains that are necessary for TNL cell death signaling. Our data suggest that TNL-triggered cell death and pathogen growth restriction are determined by distinctive features of EDS1-SAG101 and EDS1-PAD4 complexes and that these signaling machineries coevolved with further components within plant species or clades to regulate downstream pathways in TNL immunity.
Original languageEnglish
Pages (from-to)2430-2455
JournalThe Plant Cell
Volume31
Early online date16 Jul 2019
DOIs
Publication statusPublished - Oct 2019

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