The Rice Resistance Protein Pair RGA4/RGA5 Recognizes the <i>Magnaporthe oryzae</i> Effectors AVR-Pia and AVR1-CO39 by Direct Binding

Césari, Stella; Thilliez, Gaëtan; Ribot, Cécile; Chalvon, Véronique; Michel, Corinne; Jauneau, Alain; Rivas, Susana; Alaux, Ludovic; Kanzaki, Hiromitsu; Okuyama, Yudai; Morel, Jean-Benoît; Fournier, Elisabeth; Tharreau, Didier; Terauchi, Ryohei; Kroj, Thomas

doi:10.1105/tpc.112.107201

Cited by 472 publications

(521 citation statements)

References 72 publications

Supporting

Mentioning

509

Contrasting

Unclassified

Order By: Relevance

“…1b). This apparent flexibility in the integration of additional domains in NLRs had already been reported for the integration of the RATX1/HMA domain in the rice blast resistance NLRs RGA5 and Pik‐1 where it is located, respectively, at the C‐terminus or between the CC and the NB domains (Kanzaki et al ., 2012; Cesari et al ., 2013). …”

Section: Resultsmentioning

confidence: 99%

“…The first experimental evidence was provided by the investigation of the rice blast resistance NLR pairs RGA4/RGA5 and Pik‐1/Pik‐2 and important validation was supplied by detailed analysis of the A. thaliana NLR pair RPS4/RRS1 (Kanzaki et al ., 2012; Cesari et al ., 2013; Le Roux et al ., 2015; Sarris et al ., 2015). The occurrence of NLRs with decoy domains in phylogenetically unrelated immune receptors from monocot and dicot plants suggested that it is a widespread phenomenon and the first large‐scale analysis showed that the integration of unusual domains is frequent among cloned R proteins of the NLR class and RGA homologs similar to RGA5 and RRS1 (Césari et al ., 2014).…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

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

et al. 2016

Self Cite

View full text Add to dashboard Cite

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.

show abstract

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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

et al. 2016

Self Cite

View full text Add to dashboard Cite

show abstract

“…Consistent with previous reports, MLA10 :HA and MLA10 :CFP also induced a strong cell-death response. A positive control protein, the rice autoactive CC-NLR RGA4, produced a strong cell-death response, but its inactive T 500 M/Y 501 H/G 502 D mutant (rga4 TYG/MHD ) did not (16,17). Expression of the CC-NB fragments of Sr33 (residues 1-225), Sr50 (1-228), and MLA10 (1-225) also triggered a cell-death response (Fig.…”

Section: Resultsmentioning

confidence: 99%

Cytosolic activation of cell death and stem rust resistance by cereal MLA-family CC–NLR proteins

Césari¹,

Moore²,

Chen³

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

107

120

View full text Add to dashboard Cite

Plants possess intracellular immune receptors designated “nucleotide-binding domain and leucine-rich repeat” (NLR) proteins that translate pathogen-specific recognition into disease-resistance signaling. The wheat immune receptors Sr33 and Sr50 belong to the class of coiled-coil (CC) NLRs. They confer resistance against a broad spectrum of field isolates of Puccinia graminis f. sp. tritici, including the Ug99 lineage, and are homologs of the barley powdery mildew-resistance protein MLA10. Here, we show that, similarly to MLA10, the Sr33 and Sr50 CC domains are sufficient to induce cell death in Nicotiana benthamiana. Autoactive CC domains and full-length Sr33 and Sr50 proteins self-associate in planta. In contrast, truncated CC domains equivalent in size to an MLA10 fragment for which a crystal structure was previously determined fail to induce cell death and do not self-associate. Mutations in the truncated region also abolish self-association and cell-death signaling. Analysis of Sr33 and Sr50 CC domains fused to YFP and either nuclear localization or nuclear export signals in N. benthamiana showed that cell-death induction occurs in the cytosol. In stable transgenic wheat plants, full-length Sr33 proteins targeted to the cytosol provided rust resistance, whereas nuclear-targeted Sr33 was not functional. These data are consistent with CC-mediated induction of both cell-death signaling and stem rust resistance in the cytosolic compartment, whereas previous research had suggested that MLA10-mediated cell-death and disease resistance signaling occur independently, in the cytosol and nucleus, respectively.

show abstract

“…17). Rice RGA4 and RGA5 form a NB-LRR pair for recognition of Avr-Pia and Avr1-CO39, two effectors from the fungal pathogen Magnaporthe oryzae 18 . Tobacco N requires the 'N-required gene' NRG1 (ref.…”

mentioning

confidence: 99%

Two linked pairs of Arabidopsis TNL resistance genes independently confer recognition of bacterial effector AvrRps4

et al. 2015

View full text Add to dashboard Cite

Plant immunity requires recognition of pathogen effectors by intracellular NB-LRR immune receptors encoded by Resistance (R) genes. Most R proteins recognize a specific effector, but some function in pairs that recognize multiple effectors. Arabidopsis thaliana TIR-NB-LRR proteins RRS1-R and RPS4 together recognize two bacterial effectors, AvrRps4 from Pseudomonas syringae and PopP2 from Ralstonia solanacearum. However, AvrRps4, but not PopP2, is recognized in rrs1/rps4 mutants. We reveal an R gene pair that resembles and is linked to RRS1/RPS4, designated as RRS1B/RPS4B, which confers recognition of AvrRps4 but not PopP2. Like RRS1/RPS4, RRS1B/RPS4B proteins associate and activate defence genes upon AvrRps4 recognition. Inappropriate combinations (RRS1/RPS4B or RRS1B/RPS4) are non-functional and this specificity is not TIR domain dependent. Distinct putative orthologues of both pairs are maintained in the genomes of Arabidopsis thaliana relatives and are likely derived from a common ancestor pair. Our results provide novel insights into paired R gene function and evolution.

show abstract

The Rice Resistance Protein Pair RGA4/RGA5 Recognizes the Magnaporthe oryzae Effectors AVR-Pia and AVR1-CO39 by Direct Binding

Cited by 472 publications

References 72 publications

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

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

Cytosolic activation of cell death and stem rust resistance by cereal MLA-family CC–NLR proteins

Two linked pairs of Arabidopsis TNL resistance genes independently confer recognition of bacterial effector AvrRps4

Contact Info

Product

Resources

About