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Article ; Online: Subcellular localization requirements and specificities for plant immune receptor Toll‐interleukin‐1 receptor signaling

Bernoux, Maud / Chen, Jian / Zhang, Xiaojiao / Newell, Kim / Hu, Jian / Deslandes, Laurent / Dodds, Peter

The Plant Journal. 2023 June, v. 114, no. 6 p.1319-1337

2023

Abstract: 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) ... ...

Abstract	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 Ca²⁺ 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.
Keywords	Arabidopsis thaliana ; Nicotiana benthamiana ; calcium ; cell death ; cytosol ; enzyme activity ; flax ; immunologic receptors ; oligomerization ; pathogens ; phenotype ; seedlings
Language	English
Dates of publication	2023-06
Size	p. 1319-1337.
Publishing place	John Wiley & Sons, Ltd
Document type	Article ; Online
Note	JOURNAL ARTICLE
ZDB-ID	1088037-9
ISSN	1365-313X ; 0960-7412
ISSN (online)	1365-313X
ISSN	0960-7412
DOI	10.1111/tpj.16195
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Immunoprecipitation Under Non-Denaturing or Denaturing Conditions of Lysine-Acetylated Proteins Expressed in Planta.

Escouboué, Maxime / Deslandes, Laurent

Methods in molecular biology (Clifton, N.J.)

2019 Volume 1991, Page(s) 13–21

Abstract: Protein lysine acetylation is a highly conserved posttranslational modification that plays key roles in many biological processes such as the regulation of gene expression, chromatin dynamics, and metabolic pathways. Recent studies revealed that various ... ...

Abstract	Protein lysine acetylation is a highly conserved posttranslational modification that plays key roles in many biological processes such as the regulation of gene expression, chromatin dynamics, and metabolic pathways. Recent studies revealed that various pathogens use lysine acetylation to interfere with host immune responses. Identification of lysine-acetylated host proteins resulting from virulence activities of pathogen effectors is therefore essential for understanding their biological functions. Here we provide a method for immunoprecipitating lysine-acetylated proteins transiently expressed in planta under non-denaturing or denaturing conditions and detecting them by immunoblotting. To illustrate this rapid and simple procedure, immunoprecipitation of the lysine-acetylated WRKY domain of the RRS1-R immune receptor, a substrate of the Ralstonia solanacearum PopP2 effector, is presented as a typical example.
MeSH term(s)	Acetylation ; Arabidopsis/metabolism ; Arabidopsis/microbiology ; Arabidopsis Proteins/chemistry ; Arabidopsis Proteins/metabolism ; Bacterial Proteins/metabolism ; Immunoprecipitation/methods ; Lysine/chemistry ; Plant Diseases/microbiology ; Protein Denaturation ; Protein Processing, Post-Translational ; Ralstonia solanacearum/pathogenicity
Chemical Substances	Arabidopsis Proteins ; Bacterial Proteins ; Lysine (K3Z4F929H6)
Language	English
Publishing date	2019-04-30
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-4939-9458-8_2
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Article ; Online: Molecular basis for the interference of the Arabidopsis WRKY54-mediated immune response by two sequence-unrelated bacterial effectors.

Kim, Haseong / Kim, Jieun / Choi, Du Seok / Kim, Min-Sung / Deslandes, Laurent / Jayaraman, Jay / Sohn, Kee Hoon

The Plant journal : for cell and molecular biology

2024 Volume 118, Issue 3, Page(s) 839–855

Abstract: Arabidopsis thaliana WRKY proteins are potential targets of pathogen-secreted effectors. RESISTANT TO RALSTONIA SOLANACEARUM 1 (RRS1; AtWRKY52) is a well-studied Arabidopsis nucleotide-binding and leucine-rich repeat (NLR) immune receptor carrying a C- ... ...

Abstract	Arabidopsis thaliana WRKY proteins are potential targets of pathogen-secreted effectors. RESISTANT TO RALSTONIA SOLANACEARUM 1 (RRS1; AtWRKY52) is a well-studied Arabidopsis nucleotide-binding and leucine-rich repeat (NLR) immune receptor carrying a C-terminal WRKY domain that functions as an integrated decoy. RRS1-R recognizes the effectors AvrRps4 from Pseudomonas syringae pv. pisi and PopP2 from Ralstonia pseudosolanacearum by direct interaction through its WRKY domain. AvrRps4 and PopP2 were previously shown to interact with several AtWRKYs. However, how these effectors selectively interact with their virulence targets remains unknown. Here, we show that several members of subgroup IIIb of the AtWRKY family are targeted by AvrRps4 and PopP2. We demonstrate that several AtWRKYs induce cell death when transiently expressed in Nicotiana benthamiana, indicating the activation of immune responses. AtWRKY54 was the only cell death-inducing AtWRKY that interacted with both AvrRps4 and PopP2. We found that AvrRps4 and PopP2 specifically suppress AtWRKY54-induced cell death. We also demonstrate that the amino acid residues required for the avirulence function of AvrRps4 and PopP2 are critical for suppressing AtWRKY54-induced cell death. AtWRKY54 residues predicted to form a binding interface with AvrRps4 were predominantly located in the DNA binding domain and necessary for inducing cell death. Notably, one AtWRKY54 residue, E164, contributes to affinity with AvrRps4 and is exclusively present among subgroup IIIb AtWRKYs, yet is located outside of the DNA-binding domain. Surprisingly, AtWRKY54 mutated at E164 evaded AvrRps4-mediated cell death suppression. Taking our observations together, we propose that AvrRp4 and PopP2 specifically target AtWRKY54 to suppress plant immune responses.
MeSH term(s)	Arabidopsis/immunology ; Arabidopsis/genetics ; Arabidopsis/microbiology ; Arabidopsis/metabolism ; Arabidopsis Proteins/genetics ; Arabidopsis Proteins/metabolism ; Bacterial Proteins/genetics ; Bacterial Proteins/metabolism ; Cell Death ; Nicotiana/genetics ; Nicotiana/microbiology ; Nicotiana/immunology ; Nicotiana/metabolism ; Plant Diseases/microbiology ; Plant Diseases/immunology ; Plant Diseases/genetics ; Plant Immunity/genetics ; Pseudomonas syringae/pathogenicity ; Ralstonia/pathogenicity ; Ralstonia/genetics ; Ralstonia solanacearum/pathogenicity ; Transcription Factors/genetics ; Transcription Factors/metabolism
Chemical Substances	Arabidopsis Proteins ; AvrRps4 protein, Pseudomonas syringae ; Bacterial Proteins ; RRS1 protein, Arabidopsis ; Transcription Factors ; WRKY54 protein, Arabidopsis
Language	English
Publishing date	2024-01-25
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1088037-9
ISSN	1365-313X ; 0960-7412
ISSN (online)	1365-313X
ISSN	0960-7412
DOI	10.1111/tpj.16639
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Subcellular localization requirements and specificities for plant immune receptor Toll-interleukin-1 receptor signaling.

Bernoux, Maud / Chen, Jian / Zhang, Xiaoxiao / Newell, Kim / Hu, Jian / Deslandes, Laurent / Dodds, Peter

The Plant journal : for cell and molecular biology

2023 Volume 114, Issue 6, Page(s) 1319–1337

Abstract: 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) ... ...

Abstract	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
MeSH term(s)	Arabidopsis Proteins/metabolism ; DNA-Binding Proteins/genetics ; Arabidopsis/metabolism ; Receptors, Immunologic/metabolism ; Cell Death/genetics ; Plant Immunity/genetics ; Plant Diseases
Chemical Substances	Arabidopsis Proteins ; DNA-Binding Proteins ; Receptors, Immunologic ; SNC1 protein, Arabidopsis
Language	English
Publishing date	2023-04-03
Publishing country	England
Document type	Journal Article
ZDB-ID	1088037-9
ISSN	1365-313X ; 0960-7412
ISSN (online)	1365-313X
ISSN	0960-7412
DOI	10.1111/tpj.16195
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: An NLR integrated domain toolkit to identify plant pathogen effector targets.

Landry, David / Mila, Isabelle / Sabbagh, Cyrus Raja Rubenstein / Zaffuto, Matilda / Pouzet, Cécile / Tremousaygue, Dominique / Dabos, Patrick / Deslandes, Laurent / Peeters, Nemo

The Plant journal : for cell and molecular biology

2023 Volume 115, Issue 5, Page(s) 1443–1457

Abstract: Plant immune receptors, known as NOD-like receptors (NLRs), possess unique integrated decoy domains that enable plants to attract pathogen effectors and initiate a specific immune response. The present study aimed to create a library of these integrated ... ...

Abstract	Plant immune receptors, known as NOD-like receptors (NLRs), possess unique integrated decoy domains that enable plants to attract pathogen effectors and initiate a specific immune response. The present study aimed to create a library of these integrated domains (IDs) and screen them with pathogen effectors to identify targets for effector virulence and NLR-effector interactions. This works compiles IDs found in NLRs from seven different plant species and produced a library of 78 plasmid clones containing a total of 104 IDs, representing 43 distinct InterPro domains. A yeast two-hybrid assay was conducted, followed by an in planta interaction test, using 32 conserved effectors from Ralstonia pseudosolanacearum type III. Through these screenings, three interactions involving different IDs (kinase, DUF3542, WRKY) were discovered interacting with two unrelated type III effectors (RipAE and PopP2). Of particular interest was the interaction between PopP2 and ID#85, an atypical WRKY domain integrated into a soybean NLR gene (GmNLR-ID#85). Using a Förster resonance energy transfer-fluorescence lifetime imaging microscopy technique to detect protein-protein interactions in living plant cells, PopP2 was demonstrated to physically associate with ID#85 in the nucleus. However, unlike the known WRKY-containing Arabidopsis RRS1-R NLR receptor, GmNLR-ID#85 could not be acetylated by PopP2 and failed to activate RPS4-dependent immunity when introduced into the RRS1-R immune receptor. The generated library of 78 plasmid clones, encompassing these screenable IDs, is publicly available through Addgene. This resource is expected to be valuable for the scientific community with respect to discovering targets for effectors and potentially engineering plant immune receptors.
MeSH term(s)	Crops, Agricultural ; Two-Hybrid System Techniques ; Cell Nucleus ; Transcription Factors ; NLR Proteins/metabolism ; Plants/metabolism ; Plants/microbiology ; Plant Proteins/metabolism ; Gene Library
Chemical Substances	Transcription Factors ; NLR Proteins ; Plant Proteins
Language	English
Publishing date	2023-07-24
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1088037-9
ISSN	1365-313X ; 0960-7412
ISSN (online)	1365-313X
ISSN	0960-7412
DOI	10.1111/tpj.16331
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Fight hard or die trying: when plants face pathogens under heat stress

Desaint, Henri / Aoun, Nathalie / Deslandes, Laurent / Vailleau, Fabienne / Roux, Fabrice / Berthomé, Richard

new phytologist. 2021 Jan., v. 229, no. 2

2021

Abstract: In their natural environment, plants are exposed to biotic or abiotic stresses that occur sequentially or simultaneously. Plant responses to these stresses have been studied widely and have been well characterised in simplified systems involving single ... ...

Abstract	In their natural environment, plants are exposed to biotic or abiotic stresses that occur sequentially or simultaneously. Plant responses to these stresses have been studied widely and have been well characterised in simplified systems involving single plant species facing individual stress. Temperature elevation is a major abiotic driver of climate change and scenarios have predicted an increase in the number and severity of epidemics. In this context, here we review the available data on the effect of heat stress on plant–pathogen interactions. Considering 45 studies performed on model or crop species, we discuss the possible implications of the optimum growth temperature of plant hosts and pathogens, mode of stress application and temperature variation on resistance modulations. Alarmingly, most identified resistances are altered under temperature elevation, regardless of the plant and pathogen species. Therefore, we have listed current knowledge on heat‐dependent plant immune mechanisms and pathogen thermosensory processes, mainly studied in animals and human pathogens, that could help to understand the outcome of plant–pathogen interactions under elevated temperatures. Based on a general overview of the mechanisms involved in plant responses to pathogens, and integrating multiple interactions with the biotic environment, we provide recommendations to optimise plant disease resistance under heat stress and to identify thermotolerant resistance mechanisms.
Keywords	animal pathogens ; animals ; climate change ; crops ; disease outbreaks ; environment ; face ; heat stress ; heat tolerance ; host plants ; host-pathogen relationships ; knowledge ; models ; plant disease resistance ; plant response ; resistance mechanisms ; temperature
Language	English
Dates of publication	2021-01
Size	p. 712-734.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	NAL-light ; REVIEW
ZDB-ID	208885-x
ISSN	1469-8137 ; 0028-646X
ISSN (online)	1469-8137
ISSN	0028-646X
DOI	10.1111/nph.16965
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: An NLR integrated domain toolkit to identify plant pathogen effector targets

Landry, David / Mila, Isabelle / Sabbagh, Cyrus Raja Rubenstein / Zaffuto, Matilda / Pouzet, Cécile / Tremousaygue, Dominique / Dabos, Patrick / Deslandes, Laurent / Peeters, Nemo

The Plant Journal. 2023 Sept., v. 115, no. 5 p.1443-1457

2023

Abstract: Plant immune receptors, known as NOD‐like receptors (NLRs), possess unique integrated decoy domains that enable plants to attract pathogen effectors and initiate a specific immune response. The present study aimed to create a library of these integrated ... ...

Abstract	Plant immune receptors, known as NOD‐like receptors (NLRs), possess unique integrated decoy domains that enable plants to attract pathogen effectors and initiate a specific immune response. The present study aimed to create a library of these integrated domains (IDs) and screen them with pathogen effectors to identify targets for effector virulence and NLR–effector interactions. This works compiles IDs found in NLRs from seven different plant species and produced a library of 78 plasmid clones containing a total of 104 IDs, representing 43 distinct InterPro domains. A yeast two‐hybrid assay was conducted, followed by an in planta interaction test, using 32 conserved effectors from Ralstonia pseudosolanacearum type III. Through these screenings, three interactions involving different IDs (kinase, DUF3542, WRKY) were discovered interacting with two unrelated type III effectors (RipAE and PopP2). Of particular interest was the interaction between PopP2 and ID#85, an atypical WRKY domain integrated into a soybean NLR gene (GmNLR‐ID#85). Using a Förster resonance energy transfer‐fluorescence lifetime imaging microscopy technique to detect protein–protein interactions in living plant cells, PopP2 was demonstrated to physically associate with ID#85 in the nucleus. However, unlike the known WRKY‐containing Arabidopsis RRS1‐R NLR receptor, GmNLR‐ID#85 could not be acetylated by PopP2 and failed to activate RPS4‐dependent immunity when introduced into the RRS1‐R immune receptor. The generated library of 78 plasmid clones, encompassing these screenable IDs, is publicly available through Addgene. This resource is expected to be valuable for the scientific community with respect to discovering targets for effectors and potentially engineering plant immune receptors.
Keywords	Arabidopsis ; Ralstonia ; energy ; genes ; immune response ; immunologic receptors ; microscopy ; plant pathogens ; plasmids ; soybeans ; two hybrid system techniques ; virulence
Language	English
Dates of publication	2023-09
Size	p. 1443-1457.
Publishing place	John Wiley & Sons, Ltd
Document type	Article ; Online
Note	JOURNAL ARTICLE
ZDB-ID	1088037-9
ISSN	1365-313X ; 0960-7412
ISSN (online)	1365-313X
ISSN	0960-7412
DOI	10.1111/tpj.16331
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Bacterial host adaptation through sequence and structural variations of a single type III effector gene.

Lauber, Emmanuelle / González-Fuente, Manuel / Escouboué, Maxime / Vicédo, Céline / Luneau, Julien S / Pouzet, Cécile / Jauneau, Alain / Gris, Carine / Zhang, Zhi-Min / Pichereaux, Carole / Carrère, Sébastien / Deslandes, Laurent / Noël, Laurent D

iScience

2024 Volume 27, Issue 3, Page(s) 109224

Abstract: Molecular mechanisms underlying quantitative variations of pathogenicity remain elusive. Here, we identified ... ...

Abstract	Molecular mechanisms underlying quantitative variations of pathogenicity remain elusive. Here, we identified the
Language	English
Publishing date	2024-02-15
Publishing country	United States
Document type	Journal Article
ISSN	2589-0042
ISSN (online)	2589-0042
DOI	10.1016/j.isci.2024.109224
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Article ; Online: The large, diverse, and robust arsenal of Ralstonia solanacearum type III effectors and their in planta functions.

Landry, David / González-Fuente, Manuel / Deslandes, Laurent / Peeters, Nemo

Molecular plant pathology

2020 Volume 21, Issue 10, Page(s) 1377–1388

Abstract: The type III secretion system with its delivered type III effectors (T3Es) is one of the main virulence determinants of Ralstonia solanacearum, a worldwide devastating plant pathogenic bacterium affecting many crop species. The pan-effectome of the R. ... ...

Abstract	The type III secretion system with its delivered type III effectors (T3Es) is one of the main virulence determinants of Ralstonia solanacearum, a worldwide devastating plant pathogenic bacterium affecting many crop species. The pan-effectome of the R. solanacearum species complex has been exhaustively identified and is composed of more than 100 different T3Es. Among the reported strains, their content ranges from 45 to 76 T3Es. This considerably large and varied effectome could be considered one of the factors contributing to the wide host range of R. solanacearum. In order to understand how R. solanacearum uses its T3Es to subvert the host cellular processes, many functional studies have been conducted over the last three decades. It has been shown that R. solanacearum effectors, as those from other plant pathogens, can suppress plant defence mechanisms, modulate the host metabolism, or avoid bacterial recognition through a wide variety of molecular mechanisms. R. solanacearum T3Es can also be perceived by the plant and trigger immune responses. To date, the molecular mechanisms employed by R. solanacearum T3Es to modulate these host processes have been described for a growing number of T3Es, although they remain unknown for the majority of them. In this microreview, we summarize and discuss the current knowledge on the characterized R. solanacearum species complex T3Es.
MeSH term(s)	Bacterial Proteins/metabolism ; Gene Expression Profiling ; Host-Parasite Interactions ; Plant Diseases/microbiology ; Plant Immunity ; Plants/immunology ; Plants/microbiology ; Ralstonia solanacearum/pathogenicity ; Type III Secretion Systems/immunology ; Type III Secretion Systems/metabolism ; Virulence ; Virulence Factors/metabolism
Chemical Substances	Bacterial Proteins ; Type III Secretion Systems ; Virulence Factors
Language	English
Publishing date	2020-08-08
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2020755-4
ISSN	1364-3703 ; 1364-3703
ISSN (online)	1364-3703
ISSN	1364-3703
DOI	10.1111/mpp.12977
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Article: A complex network of additive and epistatic quantitative trait loci underlies natural variation of Arabidopsis thaliana quantitative disease resistance to Ralstonia solanacearum under heat stress

Aoun, Nathalie / Desaint, Henri / Boyrie, Léa / Bonhomme, Maxime / Deslandes, Laurent / Berthomé, Richard / Roux, Fabrice

Molecular plant pathology. 2020 Nov., v. 21, no. 11

2020

Abstract: Plant immunity is often negatively impacted by heat stress. However, the underlying molecular mechanisms remain poorly characterized. Based on a genome‐wide association mapping approach, this study aims to identify in Arabidopsis thaliana the genetic ... ...

Abstract	Plant immunity is often negatively impacted by heat stress. However, the underlying molecular mechanisms remain poorly characterized. Based on a genome‐wide association mapping approach, this study aims to identify in Arabidopsis thaliana the genetic bases of robust resistance mechanisms to the devastating pathogen Ralstonia solanacearum under heat stress. A local mapping population was phenotyped against the R. solanacearum GMI1000 strain at 27 and 30 °C. To obtain a precise description of the genetic architecture underlying natural variation of quantitative disease resistance (QDR), we applied a genome‐wide local score analysis. Alongside an extensive genetic variation found in this local population at both temperatures, we observed a playful dynamics of quantitative trait loci along the infection stages. In addition, a complex genetic network of interacting loci could be detected at 30 °C. As a first step to investigate the underlying molecular mechanisms, the atypical meiotic cyclin SOLO DANCERS gene was validated by a reverse genetic approach as involved in QDR to R. solanacearum at 30 °C. In the context of climate change, the complex genetic architecture underlying QDR under heat stress in a local mapping population revealed candidate genes with diverse molecular functions.
Keywords	Arabidopsis thaliana ; Ralstonia solanacearum ; climate change ; cyclins ; disease resistance ; epistasis ; genes ; genetic variation ; heat stress ; immunity ; meiosis ; pathogens ; plant pathology ; quantitative traits ; reverse genetics
Language	English
Dates of publication	2020-11
Size	p. 1405-1420.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	NAL-AP-2-clean ; JOURNAL ARTICLE
ZDB-ID	2020755-4
ISSN	1364-3703 ; 1464-6722
ISSN (online)	1364-3703
ISSN	1464-6722
DOI	10.1111/mpp.12964
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