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

Research output: Contribution to journalArticleAcademicpeer-review

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.
LanguageEnglish
Pages2430-2455
JournalThe Plant Cell
Volume31
Early online date16 Jul 2019
DOIs
Publication statusPublished - Oct 2019

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cell death
Cell Death
phytoalexins
receptors
Immunity
immunity
Plant Structures
Nicotiana benthamiana
pathogens
chimerism
Lipase
Arabidopsis
Leucine
leucine
Tobacco
Nucleotides
nucleotides
immunologic receptors
phenotype
Growth

Cite this

Lapin, D., Kovacova, V., Sun, X., Dongus, J., Bhandari, D., von Born, P., ... Parker, J. E. (2019). A coevolved EDS1-SAG101-NRG1 module mediates cell death signaling by TIR-domain immune receptors. The Plant Cell, 31, 2430-2455. https://doi.org/10.1105/tpc.19.00118
Lapin, Dmitry ; Kovacova, Viera ; Sun, Xinhua ; Dongus, Joram ; Bhandari, Deepak ; von Born, Patrick ; Bautor, Jaqueline ; Guarneri, Nina ; Rzemieniewski, Jakub ; Stuttmann, Johannes ; Beyer, Andreas ; Parker, Jane E. / A coevolved EDS1-SAG101-NRG1 module mediates cell death signaling by TIR-domain immune receptors. In: The Plant Cell. 2019 ; Vol. 31. pp. 2430-2455.
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title = "A coevolved EDS1-SAG101-NRG1 module mediates cell death signaling by TIR-domain immune receptors",
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.",
author = "Dmitry Lapin and Viera Kovacova and Xinhua Sun and Joram Dongus and Deepak Bhandari and {von Born}, Patrick and Jaqueline Bautor and Nina Guarneri and Jakub Rzemieniewski and Johannes Stuttmann and Andreas Beyer and Parker, {Jane E.}",
year = "2019",
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Lapin, D, Kovacova, V, Sun, X, Dongus, J, Bhandari, D, von Born, P, Bautor, J, Guarneri, N, Rzemieniewski, J, Stuttmann, J, Beyer, A & Parker, JE 2019, 'A coevolved EDS1-SAG101-NRG1 module mediates cell death signaling by TIR-domain immune receptors', The Plant Cell, vol. 31, pp. 2430-2455. https://doi.org/10.1105/tpc.19.00118

A coevolved EDS1-SAG101-NRG1 module mediates cell death signaling by TIR-domain immune receptors. / Lapin, Dmitry; Kovacova, Viera ; Sun, Xinhua; Dongus, Joram; Bhandari, Deepak; von Born, Patrick; Bautor, Jaqueline; Guarneri, Nina; Rzemieniewski, Jakub; Stuttmann, Johannes; Beyer, Andreas; Parker, Jane E.

In: The Plant Cell, Vol. 31, 10.2019, p. 2430-2455.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - A coevolved EDS1-SAG101-NRG1 module mediates cell death signaling by TIR-domain immune receptors

AU - Lapin, Dmitry

AU - Kovacova, Viera

AU - Sun, Xinhua

AU - Dongus, Joram

AU - Bhandari, Deepak

AU - von Born, Patrick

AU - Bautor, Jaqueline

AU - Guarneri, Nina

AU - Rzemieniewski, Jakub

AU - Stuttmann, Johannes

AU - Beyer, Andreas

AU - Parker, Jane E.

PY - 2019/10

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N2 - 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.

AB - 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.

U2 - 10.1105/tpc.19.00118

DO - 10.1105/tpc.19.00118

M3 - Article

VL - 31

SP - 2430

EP - 2455

JO - The Plant Cell

T2 - The Plant Cell

JF - The Plant Cell

SN - 1040-4651

ER -