Abstract
Plant nucleotide binding/leucine-rich repeat (NLR) immune receptors are activated by pathogen effectors to trigger host defenses and cell death. Toll-interleukin 1 receptor domain NLRs (TNLs) converge on the ENHANCED DISEASE SUSCEPTIBILITY1 (EDS1) family of lipase-like proteins for all resistance outputs. In Arabidopsis (Arabidopsis thaliana) TNL-mediated immunity, AtEDS1 heterodimers with PHYTOALEXIN DEFICIENT4 (AtPAD4) transcriptionally induced basal defenses. AtEDS1 uses the same surface to interact with PAD4-related SENESCENCE-ASSOCIATED GENE101 (AtSAG101), but the role of AtEDS1-AtSAG101 heterodimers remains unclear. We show that AtEDS1-AtSAG101 functions together with N REQUIRED GENE1 (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 and AtPAD4-AtSAG101 chimeras identify closely aligned α-helical coil surfaces in the AtEDS1-AtSAG101 partner C-terminal domains that are necessary for reconstituted 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 other components within plant species or clades to regulate downstream pathways in TNL immunity.
| Original language | English |
|---|---|
| Pages (from-to) | 2430-2455 |
| Number of pages | 26 |
| Journal | Plant Cell |
| Volume | 31 |
| Issue number | 10 |
| DOIs | |
| Publication status | Published - 2019 |
| Externally published | Yes |
Bibliographical note
Funding Information:We thank Ulla Bonas (Martin-Luther University, Halle) for the strain X. c. vesicatoria 85-10, Jeffery Dangl (University of North Carolina at Chapel Hill) fortheadr1triplemutant,LauraHerold(UniversityofZurich)forhelpingwith selection of nrg1 CRISPR lines, Artem Pankin (HHU, Düsseldorf) for helpful discussions, and Takaki Maekawa (Max-Planck Institute for Plant Breeding Research, Cologne) for providing the clone of AtADR1-L2. This work was supported by the Max-Planck Society and Deutsche Forschungsgemein-schaft (DFG) (grant CRC680 to J.E.P., D.L., V.K., A.B., CRC670 to J.E.P., D.B., and CRC648 to J.S.); DFG-ANR Trilateral ("RADAR” grant to J.E.P. and J.A.D.); the International Max-Planck Research School (doctoral fellowship to P.v.B.); and the Chinese Scholarship Council (doctoral fellowship to X.S.).
Publisher Copyright:
© 2019 ASPB.
Funding
We thank Ulla Bonas (Martin-Luther University, Halle) for the strain X. c. vesicatoria 85-10, Jeffery Dangl (University of North Carolina at Chapel Hill) fortheadr1triplemutant,LauraHerold(UniversityofZurich)forhelpingwith selection of nrg1 CRISPR lines, Artem Pankin (HHU, Düsseldorf) for helpful discussions, and Takaki Maekawa (Max-Planck Institute for Plant Breeding Research, Cologne) for providing the clone of AtADR1-L2. This work was supported by the Max-Planck Society and Deutsche Forschungsgemein-schaft (DFG) (grant CRC680 to J.E.P., D.L., V.K., A.B., CRC670 to J.E.P., D.B., and CRC648 to J.S.); DFG-ANR Trilateral ("RADAR” grant to J.E.P. and J.A.D.); the International Max-Planck Research School (doctoral fellowship to P.v.B.); and the Chinese Scholarship Council (doctoral fellowship to X.S.).