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      Integration of decoy domains derived from protein targets of pathogen effectors into plant immune receptors is widespread

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          Summary

          • Plant immune receptors of the class of nucleotide‐binding and leucine‐rich repeat domain ( NLR) proteins can contain additional domains besides canonical NB‐ARC (nucleotide‐binding adaptor shared by APAF‐1, R proteins, and CED‐4 (NB‐ARC)) and leucine‐rich repeat ( LRR) domains. Recent research suggests that these additional domains act as integrated decoys recognizing effectors from pathogens. Proteins homologous to integrated decoys are suspected to be effector targets and involved in disease or resistance.

          • Here, we scrutinized 31 entire plant genomes to identify putative integrated decoy domains in NLR proteins using the Interpro search. The involvement of the Zinc Finger–BED type (ZBED) protein containing a putative decoy domain, called BED, in rice ( Oryza sativa) resistance was investigated by evaluating susceptibility to the blast fungus Magnaporthe oryzae in rice over‐expression and knock‐out mutants.

          • This analysis showed that all plants tested had integrated various atypical protein domains into their NLR proteins (on average 3.5% of all NLR proteins). We also demonstrated that modifying the expression of the ZBED gene modified disease susceptibility.

          • This study suggests that integration of decoy domains in NLR immune receptors is widespread and frequent in plants. The integrated decoy model is therefore a powerful concept to identify new proteins involved in disease resistance. Further in‐depth examination of additional domains in NLR proteins promises to unravel many new proteins of the plant immune system.

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          See also the Commentary on this article by Malik & Van der Hoorn, 210: 371–373.

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          Most cited references23

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          A Plant Immune Receptor Detects Pathogen Effectors that Target WRKY Transcription Factors.

          Defense against pathogens in multicellular eukaryotes depends on intracellular immune receptors, yet surveillance by these receptors is poorly understood. Several plant nucleotide-binding, leucine-rich repeat (NB-LRR) immune receptors carry fusions with other protein domains. The Arabidopsis RRS1-R NB-LRR protein carries a C-terminal WRKY DNA binding domain and forms a receptor complex with RPS4, another NB-LRR protein. This complex detects the bacterial effectors AvrRps4 or PopP2 and then activates defense. Both bacterial proteins interact with the RRS1 WRKY domain, and PopP2 acetylates lysines to block DNA binding. PopP2 and AvrRps4 interact with other WRKY domain-containing proteins, suggesting these effectors interfere with WRKY transcription factor-dependent defense, and RPS4/RRS1 has integrated a "decoy" domain that enables detection of effectors that target WRKY proteins. We propose that NB-LRR receptor pairs, one member of which carries an additional protein domain, enable perception of pathogen effectors whose function is to target that domain.
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            A receptor pair with an integrated decoy converts pathogen disabling of transcription factors to immunity.

            Microbial pathogens infect host cells by delivering virulence factors (effectors) that interfere with defenses. In plants, intracellular nucleotide-binding/leucine-rich repeat receptors (NLRs) detect specific effector interference and trigger immunity by an unknown mechanism. The Arabidopsis-interacting NLR pair, RRS1-R with RPS4, confers resistance to different pathogens, including Ralstonia solanacearum bacteria expressing the acetyltransferase effector PopP2. We show that PopP2 directly acetylates a key lysine within an additional C-terminal WRKY transcription factor domain of RRS1-R that binds DNA. This disrupts RRS1-R DNA association and activates RPS4-dependent immunity. PopP2 uses the same lysine acetylation strategy to target multiple defense-promoting WRKY transcription factors, causing loss of WRKY-DNA binding and transactivating functions needed for defense gene expression and disease resistance. Thus, RRS1-R integrates an effector target with an NLR complex at the DNA to switch a potent bacterial virulence activity into defense gene activation.
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              The rice resistance protein pair RGA4/RGA5 recognizes the Magnaporthe oryzae effectors AVR-Pia and AVR1-CO39 by direct binding.

              Resistance (R) proteins recognize pathogen avirulence (Avr) proteins by direct or indirect binding and are multidomain proteins generally carrying a nucleotide binding (NB) and a leucine-rich repeat (LRR) domain. Two NB-LRR protein-coding genes from rice (Oryza sativa), RGA4 and RGA5, were found to be required for the recognition of the Magnaporthe oryzae effector AVR1-CO39. RGA4 and RGA5 also mediate recognition of the unrelated M. oryzae effector AVR-Pia, indicating that the corresponding R proteins possess dual recognition specificity. For RGA5, two alternative transcripts, RGA5-A and RGA5-B, were identified. Genetic analysis showed that only RGA5-A confers resistance, while RGA5-B is inactive. Yeast two-hybrid, coimmunoprecipitation, and fluorescence resonance energy transfer-fluorescence lifetime imaging experiments revealed direct binding of AVR-Pia and AVR1-CO39 to RGA5-A, providing evidence for the recognition of multiple Avr proteins by direct binding to a single R protein. Direct binding seems to be required for resistance as an inactive AVR-Pia allele did not bind RGA5-A. A small Avr interaction domain with homology to the Avr recognition domain in the rice R protein Pik-1 was identified in the C terminus of RGA5-A. This reveals a mode of Avr protein recognition through direct binding to a novel, non-LRR interaction domain.
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                Author and article information

                Journal
                New Phytol
                New Phytol
                10.1111/(ISSN)1469-8137
                NPH
                The New Phytologist
                John Wiley and Sons Inc. (Hoboken )
                0028-646X
                1469-8137
                05 February 2016
                April 2016
                : 210
                : 2 ( doiID: 10.1111/nph.2016.210.issue-2 )
                : 618-626
                Affiliations
                [ 1 ] INRA CIRAD SupAgroUMR BGPI INRA/CIRAD/SupAgro Campus International de Baillarguet TA A 54/K 34398 MontpellierFrance
                [ 2 ]Université Montpellier 2 Place Eugène Bataillon 34095 Montpellier Cedex 5France
                Author notes
                [*] [* ] Author for correspondence:

                Jean‐Benoit Morel

                Tel: +33 499624838

                Email: jbmorel@ 123456cirad.fr

                Article
                NPH13869 2015-20973
                10.1111/nph.13869
                5067614
                26848538
                03bae22f-7ed6-46b1-958d-b2aa8947f941
                © 2016 The Authors. New Phytologist © 2016 New Phytologist Trust

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 26 November 2015
                : 16 December 2015
                Page count
                Pages: 9
                Funding
                Funded by: CIFRE
                Funded by: Agropolis and Cariplo Fondations
                Award ID: 1201‐001
                Funded by: French ANR program ‘Investissement d'Avenir’
                Award ID: ANR‐10‐LABX‐0001‐01
                Categories
                Full Paper
                Research
                Full Papers
                Custom metadata
                2.0
                nph13869
                April 2016
                Converter:WILEY_ML3GV2_TO_NLMPMC version:4.9.5 mode:remove_FC converted:18.10.2016

                Plant science & Botany
                bed domain,decoy,genome,nucleotide‐binding and leucine‐rich repeat domain (nlr),plant immunity

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