Connecting the dots between cell surface- and intracellular-triggered immune pathways in plants

Bernoux, Maud; Zetzsche, Holger; Stuttmann, Johannes

doi:10.1016/j.pbi.2022.102276

Cited by 19 publications

(17 citation statements)

References 87 publications

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“…It is possible that the activation of effector‐independent TIR signaling (inducible expression in transgenic lines) may differ from pathogen‐delivered effector‐mediated TNL activation. Given evidence of connections and potentiation between PTI and ETI, this may explain the discrepancy (Bernoux et al., 2022).…”

Section: Discussionmentioning

confidence: 99%

“…Although cell surface and intracellular immune receptors are structurally different and localize to different subcellular compartments, their activation induces largely overlapping immune responses (reactive oxygen species production, MAPKinase cascade activation, ion fluxes, a massive transcriptional reprogramming, and sometimes the induction of cell death) (Lu & Tsuda, 2021). Increasing evidence suggest that pattern‐recognition receptor‐ and NLR‐mediated signaling pathway mutually potentiate each other (Bernoux et al., 2022).…”

Section: Introductionmentioning

confidence: 99%

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Subcellular localization requirements and specificities for plant immune receptor Toll‐interleukin‐1 receptor signaling

et al. 2023

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Recent work shed light on how plant intracellular immune receptors of the nucleotide-binding leucine-rich repeat (NLR) family are activated upon pathogen effector recognition to trigger immune responses. Activation of Toll-interleukin-1 receptor (TIR) domain-containing NLRs (TNLs) induces receptor oligomerization and close proximity of the TIR domain, which is required for TIR enzymatic activity. TIR-catalyzed small signaling molecules bind to EDS1 family heterodimers and subsequently activate downstream helper NLRs, which function as Ca 2+ permeable channel to activate immune responses eventually leading to cell death. Subcellular localization requirements of TNLs and signaling partners are not well understood, although they are required to understand fully the mechanisms underlying NLR early signaling. TNLs show diverse subcellular localization while EDS1 shows nucleocytosolic localization. Here, we studied the impact of TIR and EDS1 mislocalization on the signaling activation of different TNLs. In Nicotiana benthamiana, our results suggest that close proximity of TIR domains isolated from flax L6 and Arabidopsis RPS4 and SNC1 TNLs drives signaling activation from different cell compartments. Nevertheless, both Golgi-membrane anchored L6 and nucleocytosolic RPS4 have the same requirements for EDS1 subcellular localization in Arabidopsis thaliana. By using mislocalized variants of EDS1, we found that autoimmune L6 and RPS4 TIR domain can induce seedling cell death when EDS1 is present in the cytosol. However, when EDS1 is restricted to the nucleus, both induce a stunting phenotype but no cell death. Our data point out the importance of thoroughly investigating the dynamics of TNLs and signaling partners subcellular localization to understand TNL signaling fully.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Subcellular localization requirements and specificities for plant immune receptor Toll‐interleukin‐1 receptor signaling

et al. 2023

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“…Recent reports suggest that sensor CNLs and RNL‐type hNLRs form oligomers (resistosomes) upon activation, which can insert into membranes and function as cation‐permeable channels (Wang et al ., 2019; Bi et al ., 2021; Jacob et al ., 2021). Although it remains unclear whether resistosome formation by Arabidopsis thaliana (Arabidopsis) CNL ZAR1 (HopZ‐Activated Resistance 1) is prototypical for CNLs and RNLs, it is possible that Ca 2+ influx represents a common output in CNL and TNL‐RNL immunity (Bernoux et al ., 2022; Parker et al ., 2022).…”

Section: Introductionmentioning

confidence: 99%

EDS1 complexes are not required for PRR responses and execute TNL‐ETI from the nucleus in Nicotiana benthamiana

et al. 2022

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Heterodimeric complexes incorporating the lipase-like proteins EDS1 with PAD4 or SAG101 are central hubs in plant innate immunity. EDS1 functions encompass signal relay from TIR domain-containing intracellular NLR-type immune receptors (TNLs) towards RPW8-type helper NLRs (RNLs) and, in Arabidopsis thaliana, bolstering of signaling and resistance mediated by cell-surface pattern recognition receptors (PRRs). Increasing evidence points to the activation of EDS1 complexes by small molecule binding.We used CRISPR/Cas-generated mutant lines and agroinfiltration-based complementation assays to interrogate functions of EDS1 complexes in Nicotiana benthamiana.We did not detect impaired PRR signaling in N. benthamiana lines deficient in EDS1 complexes or RNLs. Intriguingly, in assays monitoring functions of SlEDS1-NbEDS1 complexes in N. benthamiana, mutations within the SlEDS1 catalytic triad could abolish or enhance TNL immunity. Furthermore, nuclear EDS1 accumulation was sufficient for N. benthamiana TNL (Roq1) immunity.Reinforcing PRR signaling in Arabidopsis might be a derived function of the TNL/EDS1 immune sector. Although Solanaceae EDS1 functionally depends on catalytic triad residues in some contexts, our data do not support binding of a TNL-derived small molecule in the triad environment. Whether and how nuclear EDS1 activity connects to membrane pore-forming RNLs remains unknown.

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“…Most of the plant disease-resistance genes (R genes) identified so far encode proteins of the NBS-LRR (Nucleotide Binding Site-Leucine Rich Repeat) family, which are also known as NLR proteins as the major type for the plant R gene family. The NLR protein consists of three main components: the variable N-terminal structural domain, the NB (Nucleotide-Binding) structural domain, and the C-terminal conserved LRR (leucine-richrepeat) structural domain [57,58]. Based on the characteristics of the N-terminal structural domain, NLRs are mainly divided into TNL with TIR (Toll-interleukin-1 receptor) at the N-terminal, and CNL with a CC (coiled-coil) structural domain at the N-terminal.…”

Section: Disease-resistance (R) Genes and The Nbs-lrr Protein Familymentioning

confidence: 99%

Advances in Biological Control and Resistance Genes of Brassicaceae Clubroot Disease-The Study Case of China

Zhang

et al. 2023

IJMS

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Clubroot disease is a soil-borne disease caused by Plasmodiophora brassicae. It occurs in cruciferous crops exclusively, and causes serious damage to the economic value of cruciferous crops worldwide. Although different measures have been taken to prevent the spread of clubroot disease, the most fundamental and effective way is to explore and use disease-resistance genes to breed resistant varieties. However, the resistance level of plant hosts is influenced both by environment and pathogen race. In this work, we described clubroot disease in terms of discovery and current distribution, life cycle, and race identification systems; in particular, we summarized recent progress on clubroot control methods and breeding practices for resistant cultivars. With the knowledge of these identified resistance loci and R genes, we discussed feasible strategies for disease-resistance breeding in the future.

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Connecting the dots between cell surface- and intracellular-triggered immune pathways in plants

Cited by 19 publications

References 87 publications

Subcellular localization requirements and specificities for plant immune receptor Toll‐interleukin‐1 receptor signaling

Subcellular localization requirements and specificities for plant immune receptor Toll‐interleukin‐1 receptor signaling

EDS1 complexes are not required for PRR responses and execute TNL‐ETI from the nucleus in Nicotiana benthamiana

Advances in Biological Control and Resistance Genes of Brassicaceae Clubroot Disease-The Study Case of China

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