Tackling multiple bacterial diseases of Solanaceae with a handful of immune receptors

Kim, Boyoung; Choi, Jihyun; Segonzac, Cécile

doi:10.1007/s13580-021-00415-1

Cited by 5 publications

(4 citation statements)

References 115 publications

(161 reference statements)

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“…Since X. perforans carrying avrBsT shows a reduced virulence in tomato introgression line LA4245‐R ( Ptr1 ptr1 ) (Figs 5c, S13), expressing functional Ptr1 and ZAR1 in S. lycopersicum may confer resistance against newly emerging strains of X. perforans . These genes could be stacked in tomato along with EFR from Arabidopsis, Bs2 from pepper, and Roq1 from N. benthamiana to confer durable resistance against multiple bacterial pathogens (Kunwar et al ., 2018; Thomas et al ., 2020; Kim et al ., 2022). In addition to introducing Ptr1 and ZAR1 to susceptible cultivars, further information about the host targets of the avirulence effectors including JIM2 would be useful for crop plant engineering.…”

Section: Discussionmentioning

confidence: 99%

Ptr1 and ZAR1 immune receptors confer overlapping and distinct bacterial pathogen effector specificities

Ahn,

Kim,

Choi

et al. 2023

New Phytologist

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Summary Some nucleotide‐binding and leucine‐rich repeat receptors (NLRs) indirectly detect pathogen effectors by monitoring their host targets. In Arabidopsis thaliana, RIN4 is targeted by multiple sequence‐unrelated effectors and activates immune responses mediated by RPM1 and RPS2. These effectors trigger cell death in Nicotiana benthamiana, but the corresponding NLRs have yet not been identified. To identify N. benthamiana NLRs (NbNLRs) that recognize Arabidopsis RIN4‐targeting effectors, we conducted a rapid reverse genetic screen using an NbNLR VIGS library. We identified that the N. benthamiana homolog of Ptr1 (Pseudomonas tomato race 1) recognizes the Pseudomonas effectors AvrRpt2, AvrRpm1, and AvrB. We demonstrated that recognition of the Xanthomonas effector AvrBsT and the Pseudomonas effector HopZ5 is conferred independently by the N. benthamiana homolog of Ptr1 and ZAR1. Interestingly, the recognition of HopZ5 and AvrBsT is contributed unequally by Ptr1 and ZAR1 in N. benthamiana and Capsicum annuum. In addition, we showed that the RLCK XII family protein JIM2 is required for the NbZAR1‐dependent recognition of AvrBsT and HopZ5. The recognition of sequence‐unrelated effectors by NbPtr1 and NbZAR1 provides an additional example of convergently evolved effector recognition. Identification of key components involved in Ptr1 and ZAR1‐mediated immunity could reveal unique mechanisms of expanded effector recognition.

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Section: Discussionmentioning

confidence: 99%

Ptr1 and ZAR1 immune receptors confer overlapping and distinct bacterial pathogen effector specificities

Ahn,

Kim,

Choi

et al. 2023

New Phytologist

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“…The CC‐NLR‐encoding Ptr1 gene, which was identified recently in a wild relative of tomato, S. lycopersicoides , confers resistance to Pst , Xanthomonas spp., and Ralstonia pseudosolanacearum by detecting multiple sequence‐diverse type III effectors, including AvrRpt2 (Ahn, Kim, et al., 2023; Kim et al., 2022, 2023; Mazo‐Molina et al., 2019, 2020; Tsakiri et al., 2023). It is unknown whether any Nrc protein is required for Ptr1‐mediated immunity.…”

Section: Resultsmentioning

confidence: 99%

Helper NLRs Nrc2 and Nrc3 act codependently with Prf/Pto and activate MAPK signaling to induce immunity in tomato

Zhang,

Gan,

Carneal

et al. 2023

The Plant Journal

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SUMMARYPlant intracellular immune receptors, primarily nucleotide‐binding, leucine‐rich repeat proteins (NLRs), detect pathogen effector proteins and activate NLR‐triggered immunity (NTI). Recently, ‘sensor’ NLRs have been reported to function with ‘helper’ NLRs to activate immunity. We investigated the role of two helper NLRs, Nrc2 and Nrc3, on immunity in tomato to the bacterial pathogen Pseudomonas syringae pv. tomato (Pst) mediated by the sensor NLR Prf and the Pto kinase. An nrc2/nrc3 mutant no longer activated Prf/Pto‐mediated NTI to Pst containing the effectors AvrPto and AvrPtoB. An nrc3 mutant showed intermediate susceptibility between wild‐type plants and a Prf mutant, while an nrc2 mutant developed only mild disease. These observations indicate that Nrc2 and Nrc3 act additively in Prf‐/Pto‐mediated immunity. We examined at what point Nrc2 and Nrc3 act in the Prf/Pto‐mediated immune response. In the nrc2/3 mutant, programmed cell death (PCD) normally induced by constitutively active variants of AvrPtoB, Pto, or Prf was abolished, but that induced by M3Kα or Mkk2 was not. PCD induced by a constitutively active Nrc3 was also abolished in a Nicotiana benthamiana line with reduced expression of Prf. MAPK activation triggered by expression of AvrPto in the wild‐type tomato plants was completely abolished in the nrc2/3 mutant. These results indicate that Nrc2 and Nrc3 act with Prf/Pto and upstream of MAPK signaling. Nrc2 and Nrc3 were not required for PCD triggered by Ptr1, another sensor NLR‐mediating Pst resistance, although these helper NLRs do appear to be involved in resistance to certain Pst race 1 strains

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“…The CC-NLR-encoding Ptr1 gene, which was identified recently in a wild relative of tomato, Solanum lycopersicoides, confers resistance to Pst, Xanthomonas spp. and Ralstonia pseudosolanacearum by detecting multiple sequence-diverse type III effectors, including AvrRpt2 (Mazo-Molina et al, 2019;Mazo-Molina et al, 2020;Kim et al, 2022;Ahn et al, 2023b;Kim et al, 2023;Tsakiri et al, 2023). It is unknown whether any Nrc protein is required for Ptr1-mediated immunity.…”

Section: Nrc2 and Nrc3 Do Not Play A Role In Ptr1-associated Pcdmentioning

confidence: 99%

Helper NLRs Nrc2 and Nrc3 act co-dependently with Prf/Pto and activate MAPK signaling to induce immunity in tomato

Zhang,

Gan,

Carneal

et al. 2023

Preprint

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Plant intracellular immune receptors, primarily nucleotide-binding, leucine-rich repeat proteins (NLRs), can detect virulence proteins (effectors) from pathogens and activate NLR-triggered immunity (NTI). Recently, sensor NLRs have been reported to function with helper NLRs to activate immune responses. We investigated the role of two helper NLRs, Nrc2 (NLR required for cell death 2) and Nrc3, on immunity in tomato to the bacterial pathogen Pseudomonas syringae pv. tomato (Pst) mediated by the sensor NLR Prf and the Pto kinase. Loss-of-function mutations in both Nrc2 and Nrc3 completely compromised Prf/Pto-mediated NTI to Pst containing the cognate effectors AvrPto and AvrPtoB. An nrc3 mutant showed intermediate susceptibility between wild-type tomato plants and a Prf mutant, while an nrc2 mutant developed only mild disease symptoms. These observations indicate that Nrc2 and Nrc3 act additively to contribute to Prf/Pto-mediated immunity. We also examined at what point Nrc2 and Nrc3 act in the Prf/Pto-mediated immune response. In the nrc2/3 mutant, programmed cell death (PCD) normally induced by constitutively-active variants of AvrPtoB, Pto or Prf was abolished, but that induced by M3Ka or Mkk2 was not. PCD induced by a constitutively active variant of Nrc3 was also abolished in a Nicotiana benthamiana line with reduced expression of Prf. MAPK activation triggered by expression of AvrPto in the wild-type Pto-expressing tomato plants was completely abolished in the nrc2/3 mutant. These results indicate that Nrc2 and Nrc3 act in concert with Prf/Pto and upstream of MAPK signaling. Nrc2 and Nrc3 were not required for the HR triggered by Ptr1, another sensor NLR mediating Pst resistance, although these helper NLRs do appear to be involved in resistance to certain Pst race 1 strains.

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Tackling multiple bacterial diseases of Solanaceae with a handful of immune receptors

Cited by 5 publications

References 115 publications

Ptr1 and ZAR1 immune receptors confer overlapping and distinct bacterial pathogen effector specificities

Ptr1 and ZAR1 immune receptors confer overlapping and distinct bacterial pathogen effector specificities

Helper NLRs Nrc2 and Nrc3 act codependently with Prf/Pto and activate MAPK signaling to induce immunity in tomato

Helper NLRs Nrc2 and Nrc3 act co-dependently with Prf/Pto and activate MAPK signaling to induce immunity in tomato

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